No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Scaling up our Understanding of Non-Consumptive Effects in Insect Systems
Abstract
Non-consumptive effects (NCEs) of predators on prey is an important topic in insect ecology with potential applications for pest management. NCEs are changes in prey behavior and physiology that aid in predation avoidance. While NCEs can have positive outcomes for prey survival there may also be negative consequences including increased stress and reduced growth. These effects can cascade through trophic systems influencing ecosystem function. Most NCEs have been studied at small spatial and temporal scales. However, recent studies show promise for the potential to manipulate NCEs for pest management. We suggest the next frontier for NCE studies includes manipulating the landscape of fear to improve pest control, which requires scaling-up to field and landscape levels, over ecologically relevant time frames.
... Predator-prey interactions can have direct consumptive, and indirect non-consumptive effects. Nonconsumptive predator effects refer to reductions in prey tness through behavioural and physiological changes [30][31][32][33] . The direction and intensity of non-consumptive predator effects may vary depending on the characteristics of the predator-prey couple, for example the predator:prey body size ratio which determines predator gape limitation 34 . ...
... It has been demonstrated that non-consumptive predator effects can change prey life history traits 32,115,116 , and could therefore potentially weaken or remove SMPE in prey, by, for example, reduced foraging rate in prey due to predator avoidance [117][118][119] . Here, we show that predator cues affected damsel y life history, but without having an effect on SMPEs. ...
... We suggest that the impact of these two factors were offset by antagonistic larval interactions. Antagonistic interactions can change larval behavior to avoid predation32 . Previous studies ...
Differences in hatching dates can shape intraspecific interactions through size-mediated priority effects (SMPE), a phenomenon where bigger, early hatched individuals gain advantage over smaller, late hatched ones. However, it remains unclear to what extent and how SMPE are affected by key environmental factors such as warming and predation risk imposed by top predators. We studied effects of warming (low and high temperature) and predation risk (presence and absence of predator cues of perch) on SMPE in life history and physiological traits in the cannibalistic damselfly Ischnura elegans . We induced SMPE in the laboratory by manipulating hatching dates, creating following groups: early and late hatchlings reared in separate containers, and mixed phenology groups where early and late hatchlings shared the same containers. We found strong SMPE for survival and emergence success, with the highest values in early larvae of mixed phenology groups and the lowest values in late larvae of mixed phenology groups. Neither temperature nor predator cues affected SMPE for these two traits. The other life history traits (development rate and mass at emergence) did not show SMPE, but were affected by temperature and predator cues. A tendency for SMPE was found for protein content, in the high temperature treatment. The other physiological traits (phenoloxidase activity and fat content) showed fixed expressions across treatments, indicating decoupling between physiology and life history. The results underline that SMPEs are trait-dependent, and only weakly or not affected by temperature and predation risk.
... These trophic dynamics can be generalized into two categories: consumptive and non-consumptive effects. Consumptive effects describe prey mortality from predation, while enemy-risk or non-consumptive effects describe a reduction in prey fitness associated with the costs of risk-induced behavioral changes [1][2][3]. For example, pea aphids drop from plants to escape predators such as ladybugs. ...
... Plants can play an important role in the severity of enemy-risk effects [2]. For instance, grasshoppers, which mostly feed on grass in the absence of predators, fed on less nutritious forbs when they were exposed to spiders. ...
... The fact that exposure to parasitoids in the larval stage carries over to influence adult size, which is often correlated with fecundity, suggests that enemy-risk effects may impact DBM population dynamics. Future studies should focus on larger-scale impacts of enemy-risk effects on DBM, including increasing temporal scales over multiple generations and spatial scales in agricultural fields [2,5]. Intercropping with plants that maximize enemy-risk effects on DBM could potentially enhance biological control efforts. ...
Enemy-risk effects (i.e., non-consumptive effects) describe the non-lethal fitness costs incurred by animals when they perceive a risk of predation. These effects can result from fear-associated changes in behavior and physiology. Diamondback moth larvae (Plutella xylostella) are known to violently wriggle backwards and drop from their host plants, usually suspending themselves with a silk thread, when threatened by predators and parasitoids. Here, we investigated the developmental costs associated with this behavior when larvae were exposed to its specialist parasitoid wasp (Diadegma insulare). Additionally, the structural and chemical properties of plants are well-known to influence predation and parasitism rates of herbivorous insects. Yet, few studies have examined the influence of plants on enemy-risk effects. Therefore, we examined the developmental costs associated with parasitism risk on two host plants. Diamondback moth larvae were placed on either cabbage or Virginia pepperweed plants and exposed to gravid parasitoids with truncated ovipositors, which prevented piercing of the host cuticle without affecting host searching and attacking behaviors. On Virginia pepperweed, risk of parasitism resulted in reduced larval weight gain, longer development time, and smaller adult size compared to larvae that were not exposed to parasitoids. However, on cabbage, parasitoid exposure prolonged development time but had no significant effects on larval weight gain and adult size. On both plants, parasitoid-exposed larvae were found feeding on older foliage than younger foliage. Our findings demonstrate that the enemy-escape behavior of diamondback moths has developmental costs and that plants may mediate the intensity of these enemy-risk effects.
... Facing strong natural enemies' selection, they have evolved various defense strategies, such as acquiring protections against predators, pathogens and parasitoids through association with symbiotic bacteria (Sanders et al. 2016;Ramírez-Cáceres et al. 2019;Vorburger 2022). Recent advances in insect community ecology showed that predatorprey interactions have important implications for insect pest management (Hermann & Landis 2017). Previous literatures on symbiotic bacteria mainly focused on their direct effects (i.e., consumptive effects; CEs) on the interactions between hosts and predators, although non-consumptive effects (i.e., predator-mediated effects in prey behavior and physiology that do not involve direct consumption; NCEs) were identified as be equally or more significant in the change of prey population dynamic than CEs (Hermann & Landis 2017). ...
... Recent advances in insect community ecology showed that predatorprey interactions have important implications for insect pest management (Hermann & Landis 2017). Previous literatures on symbiotic bacteria mainly focused on their direct effects (i.e., consumptive effects; CEs) on the interactions between hosts and predators, although non-consumptive effects (i.e., predator-mediated effects in prey behavior and physiology that do not involve direct consumption; NCEs) were identified as be equally or more significant in the change of prey population dynamic than CEs (Hermann & Landis 2017). In addition, understanding of how NCEs alter predator-prey dynamics was crucial to understand ecosystem and community dynamics (Sanders et al. 2016;Hermann & Landis 2017). ...
... Previous literatures on symbiotic bacteria mainly focused on their direct effects (i.e., consumptive effects; CEs) on the interactions between hosts and predators, although non-consumptive effects (i.e., predator-mediated effects in prey behavior and physiology that do not involve direct consumption; NCEs) were identified as be equally or more significant in the change of prey population dynamic than CEs (Hermann & Landis 2017). In addition, understanding of how NCEs alter predator-prey dynamics was crucial to understand ecosystem and community dynamics (Sanders et al. 2016;Hermann & Landis 2017). Therefore, the study of NCEs on prey population dynamics needs more attention. ...
Previous studies have shown that Regiella insecticola modulated the parasitism rate in wheat aphid, Sitobion miscanthi. However, little is known about influences of the symbiont on wheat aphids by predators, the other important strategy used in biological control. Herein, we in the study examined effects of the R. insecticola on aphid population dynamics under non-consumptive effects, and predation of S. miscanthi under consumptive effects of the ladybeetle Harmonia axyridis, a major predator in field populations. The results showed that i) without exposure to the predator, R. insecticola led to an increase in aphid populations (e.g., higher intrinsic rate of increase); ii) compared to without exposure to the predator, the short-term exposure (i.e., 4 h) increased aphid populations (either symbiont infection or not), whereas a contrary result was observed under the relatively long-term exposure (i.e., 24 h); iii) compared to symbiont-free aphids, symbiotic aphids did improve defenses against H. axyridis in the consumptive assay, and mainly attributing to the increase of handling time (Th ) of the predator to symbiotic aphids. The study provides new insights on the roles of symbionts on biological control by predators and insect population dynamics.
... In pest control, nonconsumptive effects of natural enemies can increase pest risk and reduce pest damage by magnitudes comparable with consumptive interactions (Eubanks & Finke, 2014;Hermann & Landis, 2017;Thaler & Griffin, 2008). These interactions can have effects on pest populations that are disproportionate to the density of natural enemies, potentially serving as mechanisms for the influence of keystone biocontrol agents (Meadows et al., 2017). ...
... Other research on aphid dropping in multiple wasp enemy communities has found more conflicting results, in which consumptive effects between enemies resulted in interference and reduced overall prey suppression, but nonconsumptive effects yielded positive additive prey suppression (Ingerslew & Finke, 2018). Despite this research, few studies have explored the importance of nonconsumptive interactions in multienemy pest control scenarios, in which impacts on crop damage are explicitly tested (Hermann & Landis, 2017). Furthermore, the dynamics of nonconsumptive interactions are not well understood in pest control, and few studies have tested how nonconsumptive enemy behavior changes across space or time (Hermann & Landis, 2017;Sheriff et al., 2018), despite the long history of dynamical research on consumptive predator-prey interactions. ...
... Despite this research, few studies have explored the importance of nonconsumptive interactions in multienemy pest control scenarios, in which impacts on crop damage are explicitly tested (Hermann & Landis, 2017). Furthermore, the dynamics of nonconsumptive interactions are not well understood in pest control, and few studies have tested how nonconsumptive enemy behavior changes across space or time (Hermann & Landis, 2017;Sheriff et al., 2018), despite the long history of dynamical research on consumptive predator-prey interactions. This may be particularly important when nonconsumptive effects are driven by predator aggression, as opposed to prey behavioral responses, and spatial or temporal variation in alternative resources for predators impacts the strength of nonconsumptive effects, potentially resulting in variable or inconsistent pest damage suppression. ...
Natural pest control is an alternative to pesticide use in agriculture, which may help to curb insect declines and promote crop production. Nonconsumptive interactions in natural pest control, which historically have received far less attention than consumptive interactions, may have distinct impacts on pest damage suppression and may also mediate positive multipredator interactions. Additionally, when nonconsumptive effects are driven by natural enemy aggression, variation in alternative resources for enemies may impact the strength of pest control. Here we study control of the coffee berry borer (CBB), Hypothenemus hampei, by a keystone arboreal ant species, Azteca sericeasur, which exhibits a nonconsumptive effect on CBB by throwing them off coffee plants. We conducted two experiments to investigate: 1) if the strength of this behavior is driven by spatial or temporal variability in scale insect density (an alternative resource which Azteca tends for honeydew), 2) if this behavior mediates positive interactions between Azteca and other ground‐foraging ants, and 3) the effect this behavior has on the overall suppression of CBB damage in multipredator scenarios. Our behavioral experiment showed that nearly all interactions between Azteca and CBB are nonconsumptive and that this behavior occurs more frequently in the dry season and with higher densities of scale insects on coffee branches. Our multipredator experiment revealed that borers thrown off coffee plants by Azteca can survive and potentially damage other nearby plants but may be suppressed by ground‐foraging ants. Although we found no non‐additive effects between Azteca and ground‐foraging ants on overall CBB damage, together, both species resulted in the lowest level of plant damage with the subsequent reduction in “spillover” damage caused by thrown CBB, indicating spatial complementarity between predators. These results present a unique case of natural pest control, where damage suppression is driven almost exclusively by nonconsumptive natural enemy aggression, as opposed to consumption or prey behavioral changes. Furthermore, our results demonstrate the variability that may occur in nonconsumptive pest control interactions when natural enemy aggressive behavior is impacted by alternative resources, and also show how these nonconsumptive effects can mediate positive interactions between natural enemies to enhance overall crop damage reduction.
... Non-consumptive effects (NCEs) are forms of indirect relationships existing between predators and their prey (Thaler and Griffin 2008;Hermann and Landis 2017;Stephan et al. 2017). NCEs can influence behavior, e.g. ...
... NCEs can influence behavior, e.g. reduce activity or feeding, increase refuge use (Hermann and Landis 2017), life history, e.g. change development time (Stoks 2001;Xiong et al. 2015), or morphological traits, e.g. ...
... NCEs have been well-studied in aquatic and terrestrial systems (Werner and Peacor 2003;Benard 2004;Ferrari et al. 2010;Breviglieri et al. 2017;Say-Sallaz et al. 2019), in both insect (Hermann and Landis 2017) and non-insect groups (Dennis et al. 2010;Auld and Relyea 2011). Most studies have revealed the roles of odor or visual cues in mediating NCEs (Wisenden 2000;Ferrari et al. 2010;Hermann and Thaler 2014;Hermann and Landis 2017;Pears et al. 2018;Arteaga-Torres et al. 2020). ...
Prey can detect the presence of predators by predator-released cues and then flexibly alter their phenotypical traits to mitigate the risk, thus non-consumptive effects emerge. Non-consumptive effects have been widely studied in many ecosystems, however, the mechanisms underlying these effects are poorly understood, leaving questions as to the nature of the risk cues and how prey detect the predator. Here, we used a Y-tube olfactometer to examine whether small brown planthoppers, Laodelphax striatellus (Fallén), could detect the presence of rove beetles (Paederus fuscipes Curtis) via odor from rove beetle abdominal gland secretion. We further identified the chemicals of abdominal gland secretion by gas chromatography-mass spectrometry. Chemicals identified were exposed to a planthopper to test their effects on planthopper behavior. Female or male planthoppers could distinguish the predation risk odors of rove beetle or rove beetle abdominal gland secretion from odor without predation risks. Through gas chromatography-mass spectrometry, sixteen of the most abundant chemicals were found in female and male abdominal gland secretion. Five of them (n-undecane, n-pentadecane, n-hexadecane, n-eicosane, and n-heneicosane) individually or collectively reduced the activity level of planthoppers. These findings enhance our understanding of the role of abdominal gland secretion in mediating non-consumptive predator effects, with significant implications for pest management, and the evolution of chemical signals.
... In general, non-consumptive effects are considered common and can produce direct and indirect effects on herbivores and plants that are as strong as and sometimes stronger than consumptive effects [4]. However, a review of non-consumptive studies involving arthropods found that over half of the studies were completed in under 24 hours and only one third lasted for more than one week [5]. Thus, our understanding of how non-consumptive effects influence predator-prey population dynamics is largely based on studies that are limited to a single predator and/or prey generation, and often less [5,6]. ...
... However, a review of non-consumptive studies involving arthropods found that over half of the studies were completed in under 24 hours and only one third lasted for more than one week [5]. Thus, our understanding of how non-consumptive effects influence predator-prey population dynamics is largely based on studies that are limited to a single predator and/or prey generation, and often less [5,6]. ...
... Non-consumptive suppression of prey by predators is well documented, but our understanding of the importance of non-consumptive effects for predator-prey interactions is limited by the short duration of most experimental studies [5]. This is partly due to the logistical difficulty of creating treatments that tease apart non-consumptive from consumptive effects in a manner that will persist across predator generations. ...
Understanding the factors that influence predator-prey dynamics requires an investigation of oscillations in predator and prey population sizes over time. However, empirical studies are often performed over one or fewer predator generations. This is particularly true for studies addressing the non-consumptive effects of predators on prey. In a previous study that lasted less than one predator generation, we demonstrated that two species of parasitoid wasps additively suppressed aphid populations through a combination of consumptive and non-consumptive effects. However, the non-consumptive effects of one wasp reduced the reproductive success of the other, suggesting that a longer-term experiment may have revealed antagonism between the wasps. The goal of our current study is to evaluate multi-generation consumptive and non-consumptive interactions between pea aphids ( Acyrthosiphon pisum ) and the wasps Aphidius ervi and Aphidius colemani . Aphidius ervi is a common natural enemy of pea aphids. Aphidius colemani is a non-consumptive enemy that does not consume pea aphids, but negatively affects pea aphid performance through behavioral disturbance. Large field cages were installed to monitor aphid abundance in response to the presence and absence of both species of wasp over four weeks (two parasitoid generations). We found that the non-consumptive enemy A . colemani initially controlled the pea aphid population, but control in the absence of parasitism was not sustainable over the long term. Aphidius ervi suppressed pea aphids through a combination of consumptive and non-consumptive effects. This suppression was more effective than that of A . colemani , but aphid abundance fluctuated over time. Suppression by A . ervi and A . colemani together was complementary, leading to the most effective and stable control of pea aphids. Therefore, promoting a diverse natural enemy community that contributes to pest control through consumptive and non-consumptive interactions may enhance the stability of herbivore population suppression over time.
... It can be difficult to scale up enemy-risk effect studies from measuring pest responses to the measures of biocontrol efficacy, including effects on pest population dynamics or crop yield, as these typically require longer timescales and broader spatial scales (Hermann and Landis, 2017). However, when moving from pest-agent interactions to the harvest and sale of a crop, there are many steps where the enemy-risk effects may attenuate (Hamburg and Hassell, 1984;Godfray and Waage, 1991;Collier and Van Steenwyk, 2004;Kaplan et al., 2014). ...
... Enemy-risk effects and direct consumptive effects frequently occur on different spatiotemporal scales, with many risk effects occurring over larger areas and longer times than CEs. This means that many studies focusing on CEs lack the scale necessary to capture enemy-risk effects, a topic that has been reviewed elsewhere (Hermann and Landis, 2017) and covered with respect to biological control in Table 2. Beyond expanding the scales of biocontrol enemy-risk effect research in the future, current theory and evidence from the broader literature may help biocontrol practitioners conceptualise and predict how enemy risk affects pest abundance and interactions with other pest management measures in time and space. ...
... Furthermore, if the focus of a study is solely on shortterm effects, these long-term changes may not be measured. Similarly, if long-term population growth is studied without looking at short-term mechanisms, NCEs might be missed entirely, and the change in growth rate may be attributed solely to CEs (see Hermann and Landis, 2017 for a more in depth discussion of appropriate timescales). ...
Enemy-risk effects, often referred to as non-consumptive effects (NCEs), are an important feature of predator-prey ecology, but their significance has had little impact on the conceptual underpinning or practice of biological control. We provide an overview of enemy-risk effects in predator-prey interactions, discuss ways in which risk effects may impact biocontrol programs and suggest avenues for further integration of natural enemy ecology and integrated pest management. Enemy-risk effects can have important influences on different stages of biological control programs, including natural enemy selection, efficacy testing and quantification of non-target impacts. Enemy-risk effects can also shape the interactions of biological control with other pest management practices. Biocontrol systems also provide community ecologists with some of the richest examples of behaviourally mediated trophic cascades and demonstrations of how enemy-risk effects play out among species with no shared evolutionary history, important topics for invasion biology and conservation. We conclude that the longstanding use of ecological theory by biocontrol practitioners should be expanded to incorporate enemy-risk effects, and that community ecologists will find many opportunities to study enemy-risk effects in biocontrol settings.
... We suggest that the impact of these two factors were offset by antagonistic larval interactions. Antagonistic interactions can change larval behavior to avoid predation 32 . Previous studies showed that life history traits in damselflies are altered by non-consumptive predator stress 33,53,64,[82][83][84] and temperature 53,85,86 . ...
... It has been demonstrated that non-consumptive predator effects can change prey life history traits 32,115,116 , and could therefore potentially weaken or remove SMPE in prey, by, for example, reduced foraging rate in prey due to predator avoidance [117][118][119] . Here, we show that predator cues affected damselfly life history, but without having an effect on SMPEs. ...
Differences in hatching dates can shape intraspecific interactions through size-mediated priority effects (SMPE), a phenomenon where bigger, early hatched individuals gain advantage over smaller, late hatched ones. However, it remains unclear to what extent and how SMPE are affected by key environmental factors such as warming and predation risk imposed by top predators. We studied effects of warming (low and high temperature) and predation risk (presence and absence of predator cues of perch) on SMPE in life history and physiological traits in the cannibalistic damselfly Ischnura elegans. We induced SMPE in the laboratory by manipulating hatching dates, creating following groups: early and late hatchlings reared in separate containers, and mixed phenology groups where early and late hatchlings shared the same containers. We found strong SMPE for survival and emergence success, with the highest values in early larvae of mixed phenology groups and the lowest values in late larvae of mixed phenology groups. Neither temperature nor predator cues affected SMPE for these two traits. The other life history traits (development rate and mass at emergence) did not show SMPE, but were affected by temperature and predator cues. A tendency for SMPE was found for protein content, in the high temperature treatment. The other physiological traits (phenoloxidase activity and fat content) showed fixed expressions across treatments, indicating decoupling between physiology and life history. The results underline that SMPEs are trait-dependent, and only weakly or not affected by temperature and predation risk.
... Predators can also have non-consumptive effects on prey (Peacor and Werner, 2001), and these effects are thought to be more pronounced in aquatic ecosystems than in terrestrial ecosystems (Preisser et al., 2005). Non-consumptive effects of predators are the result of the prey initiating antipredator behavioral and/or physiological trait changes that can aid in predator avoidance (Hermann and Landis, 2017;Lima and Dill, 1990). Such plasticity in certain prey traits may also result in energetic costs (Lima, 1998). ...
... The oviposition response to predation is expected to be weakest among Aedes species that oviposit above the water line, due in part to their delayedhatching eggs (Vonesh and Blaustein, 2010). Predation is predicted to reduce mosquito size and lengthen development time, consistent with the reduced growth response observed in other insect systems (Hermann and Landis, 2017). Certain non-consumptive effects of predation, particularly oviposition site selection and decreased vector size, are likely to play important roles in the dynamics of mosquito-borne disease. ...
Predator-prey interactions influence prey traits through both consumptive and non-consumptive effects, and variation in these traits can shape vector-borne disease dynamics. Meta-analysis methods were employed to generate predation effect sizes by different categories of predators and mosquito prey. This analysis showed that multiple families of aquatic predators are effective in consumptively reducing mosquito survival, and that the survival of Aedes, Anopheles, and Culex mosquitoes is negatively impacted by consumptive effects of predators. Mosquito larval size was found to play a more important role in explaining the heterogeneity of consumptive effects from predators than mosquito genus. Mosquito survival and body size were reduced by non-consumptive effects of predators, but development time was not significantly impacted. In addition, Culex vectors demonstrated predator avoidance behavior during oviposition. The results of this meta-analysis suggest that predators limit disease transmission by reducing both vector survival and vector size, and that associations between drought and human West Nile virus cases could be driven by the vector behavior of predator avoidance during oviposition. These findings are likely to be useful to infectious disease modelers who rely on vector traits as predictors of transmission.
... The role of predation risk on anti-predator decision making by prey and resulting non-consumptive effects have been demonstrated primarily in aquatic insect and fish systems as well as in several terrestrial mammalian systems (Preisser et al. 2005), leaving much to be explored in terrestrial insects (Hermann and Landis 2017). Among insects, aphids represent a unique group with a complex life-history. ...
... In addition, we show that several prey traits are influenced by predator odor cues, all of which are important for the success of individual aphids and could scale to interfere with the success of the population. Our study further suggests the important role of predator chemical cues in predation risk related non-consumptive effects (Gonthier 2012;Hoefler et al. 2012;Ninkovic et al. 2013;Hermann and Thaler 2014), which not only has direct implications for understanding fundamental insect ecology, but also has practical applications in pest management and conservation efforts (Hermann and Landis 2017) and shows promise in aphid systems (Ingerslew and Finke 2020). Future work must look at the adaptive potential of these shifts in behavior and physiology to determine if these trait changes ultimately aid in predator avoidance and overall survival or if they are maladaptive and lead to a net negative impact on prey population growth and success. ...
To avoid predation, prey initiate anti-predator defenses such as altered behavior, physiology and/or morphology. Prey trait changes in response to perceived predation risk can influence several aspects of prey biology that collectively contribute to individual success and thus population growth. However, studies often focus on single trait changes in a discrete life stage or morphotype. We assessed how predation risk by Harmonia axyridis affects several important traits in the aphid, Myzus persicae: host plant preference, fecundity and investment in dispersal. Importantly, we examined whether these traits changed in a similar way between winged (alate) and wingless (apterous) adult aphid morphotypes, which differ in morphology, but also in life-history characteristics important for reproduction and dispersal. Host plant preference was influenced by the presence of H.axyridis odors in choice tests; wingless aphids were deterred by the odor of plants with H.axyridis whereas winged aphids preferred plants with H.axyridis present. Wingless aphids reared in the presence of ladybeetle cues produced fewer offspring in the short-term, but significantly more when reared with exposure to predator cues for multiple generations. However, winged aphid fecundity was unaffected by H.axyridis cues. Lastly, transgenerational plasticity was demonstrated in response to predation risk via increased formation of winged aphid morphotypes in the offspring of predator cue-exposed wingless mothers. Importantly, we found that responses to risk differ across aphid polyphenism and that plasticity in aphid morphology occurs in response to predation risk. Together our results highlight the importance of considering how predation risk affects multiple life stages and morphotypes.
... Only two studies measured the risk effects of enemies on non-target species (Walzer & Schausberger 2009;Fill et al. 2012); these effects are likely overlooked in many evaluations of host range, as we discuss in the following section.f It can be difficult to scale up enemy-risk effect studies from measuring pest responses to measures of biocontrol efficacy, including effects on pest population dynamics or crop yield, as these typically require longer timescales and broader spatial scales (Hermann & Landis 2017). However, when moving from pest-agent interactions to the harvest and sale of a crop, there are many steps where the enemy-risk effects may attenuate (Hamburg & Hassell 1984;Godfray & Waage 1991;Collier & Van Steenwyk 2004;Kaplan et al. 2014). ...
... Enemy-risk effects and direct consumptive effects frequently occur on different spatiotemporal scales, with many risk effects occurring over larger areas and longer times than CEs. This means that many studies focusing on CEs lack the scale necessary to capture enemy-risk effects, a topic that has been reviewed elsewhere (Hermann & Landis 2017) and covered with respect to biological control in Table 2. Beyond expanding the scales of biocontrol enemy-risk effect research in the future, current theory and evidence from the broader literature may help biocontrol practitioners conceptualize and predict how enemy risk affects pest abundance and interactions with other pest management measures in time and space. ...
... While our findings are limited to short-term exposure, we found that prey antipredator types interacts with predator hunting mode to determine the prey metabolic responses. Most other studies on nonconsumptive predator-prey interactions employ behavioral traits such as foraging, vigilance and habitat use, or life history traits such as growth rate, survival and fecundity (Hermann and Landis 2017). These responses are then used to infer effects within individuals, and at the population and community level, which has been met with recent criticism (Peers et al. 2018). ...
Predation risk causes prey to react in numerous ways, from life history changes to shifts in habitat. These responses give some insight into how different types of predators affect prey, but prey responses are often not comparable across taxa and experimental systems. Metabolism is a ubiquitous trait among living organisms, which offers a way to examine predator effects and create generalizable outcomes. We examined metabolic responses of terrestrial and aquatic prey from three antipredator functional groups under varied contexts of predator cues. We found that constitutively defended prey did not exhibit metabolic responses to any type of predator cues, while deimatic and freeze‐flight prey exhibited metabolic responses that were dependent on both the cue type and predator hunting mode. Consistent with previous studies on nonconsumptive effects, we also found that ambush predators elicited a metabolic response while active predators did not. We propose that future work on this topic should continue to take a metabolic approach as a unified, scalable response variable to the sensory ecology of nonconsumptive effects, while identifying additional systems that can evaluate more fully both predator hunting mode and prey antipredator defenses.
... The counter-selection created by predation is a key evolutionary force in sexual selection, especially for acoustic signalling. Prey may adopt various mechanisms to avoid predators (Hermann and Landis 2017). When prey species are unable defend themselves physically or chemically, they may be more likely to develop predator avoidance strategies (Pintar et al. 2021). ...
Ecological interactions, including competition, predation, and environmental conditions, may significantly impact acoustic signalling behaviour. Here we characterise nocturnal signalling patterns in the bladder grasshopper Bullacris unicolor and relate this to biotic and abiotic factors, thus providing insights into ecological drivers of acoustic signalling behaviour. Passive acoustic recorders monitored nocturnal calling activity of the focal species, competitors, and predatory bats across the distribution of B. unicolor. Results indicate that B. unicolor calls preferentially at certain times of the night, but that peak activity period varies across the geographic range. There was a strong relationship between B. unicolor activity and bat activity. Bullacris unicolor populations further north showed an overall avoidance of bat echolocation call period, whereas further south an overlapping of call periods between B. unicolor and bat echolocation was observed. Bats at northern sites showed a distinct activity period early in the night and B. unicolor may thus reduce predation risk by shifting signalling activity to later in the night. In contrast, bats were active throughout the night at southern sites and B. unicolor did not delay calling activity in this region of its distribution, although the species did shift signalling slightly to reduce peak overlap with co-existing pneumorid species.
... Several studies have measured the non-consumptive effects of this predator, also known as "fear ecology," using either live Podisus adults with amputated mouthparts, or lures containing their synthetic aggregation pheromone (Hermann and Landis, 2017). Hermann and Thaler (2014) showed that the male-produced aggregation pheromone was responsible for the majority of the effect, which reduced feeding by 29% in the presence of nonfeeding male Podisus. ...
... However, nonconsumptive effects of predators on prey fitness and forage may also contribute to pest biological control but have been rarely evaluated. 49,50 Two recent reports shed some light on this matter using insect 51 and mammal 52 predator-prey systems, respectively. The former indicated that predator cues can significantly reduce pest fitness and suppress pest population, and the latter shows that these cues can repel the pest. ...
Background:
The success of biological control using predators is normally assumed to be achieved through direct predation. Yet it is largely unknown how the predator- and killed prey-induced stress to prey may contribute to biological control effectiveness. Here, we investigate variations in life-history traits and offspring fitness of the spider mite Tetranychus ludeni in response to cues from the predatory mite Phytoseiulus persimilis and killed T. ludeni, providing knowledge for evaluation of the nonconsumptive contribution to the biological control of T. ludeni and for future development of novel spider mite control measures using these cues.
Results:
Cues from predators and killed prey shortened longevity by 23-25% and oviposition period by 35-40%, and reduced fecundity by 31-37% in T. ludeni females. These cues significantly reduced the intrinsic rate of increase (rm ) and net population growth rate (R0 ), and extended time to double the population size (Dt ). Predator cues significantly delayed lifetime production of daughters. Mothers exposed to predator cues laid significantly smaller eggs and their offspring developed significantly more slowly but these eggs had significantly higher hatch rate.
Conclusion:
Predator- and killed prey-induced fears significantly lower the fitness of T. ludeni, suggesting that these nonconsumptive effects can contribute to the effectiveness of biological control to a great extent. Our study provides critical information for evaluation of biological control effectiveness using predators and paves the way for identification of chemical odors from the predator and killed prey, and development of new materials and methods for the control of spider mite pests. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
... The narrative has also been strengthened by researchers re-interpreting classic studies of predation in food webs as potentially being heavily influenced by risk effects (Peckarsky et al., 2008). Further, extensive experimental and theoretical literature on NCEs and TMIEs has given rise to numerous reviews in the general ecological literature (Ohgushi et al., 2012;Preisser et al., 2005;Werner & Peacor, 2003), in more specialised literatures on certain taxa or systems (e.g., Hermann & Landis, 2017;Mitchell & Harborne, 2020;Say-Sallaz et al., 2019), and on particular aspects such as context dependence [e.g., effect of prey density or environmental factors (Peacor et al., 2013;Wirsing et al., 2020)]. ...
A narrative in ecology is that prey modify traits to reduce predation risk, and the trait modification has costs large enough to cause ensuing demographic, trophic and ecosystem consequences, with implications for conservation, management and agriculture. But ecology has a long history of emphasising that quantifying the importance of an ecological process ultimately requires evidence linking a process to unmanipulated field patterns. We suspected that such process‐linked‐to‐pattern (PLP) studies were poorly represented in the predation risk literature, which conflicts with the confidence often given to the importance of risk effects. We reviewed 29 years of the ecological literature which revealed that there are well over 4000 articles on risk effects. Of those, 349 studies examined risk effects on prey fitness measures or abundance (i.e., non‐consumptive effects) of which only 26 were PLP studies, while 275 studies examined effects on other interacting species (i.e., trait‐mediated indirect effects) of which only 35 were PLP studies. PLP studies were narrowly focused taxonomically and included only three that examined unmanipulated patterns of prey abundance. Before concluding a widespread and influential role of predation‐risk effects, more attention must be given to linking the process of risk effects to unmanipulated patterns observed across diverse ecosystems.
... Besides, it may also mitigate the expected positive impact of the non-consumptive effects of predators (NCEs; Preisser et al. 2007;Sih et al. 2009) such as decreased crop damage due to reduced feeding rate in pests (Beleznai et al. 2017;Tholt et al. 2018). This inflation of NCEs due to information spread can generate discrepancies in the findings of largescale field studies and laboratory experiments (see in Weissburg et al. 2014), and should be taken into consideration in investigations that aim to evaluate how NCEs may trigger trophic cascades in different ecosystems (Hermann and Landis 2017;Haggerty et al. 2018;Pessarrodona et al. 2019). ...
Inadvertent social information (ISI) use, i.e., the exploitation of social cues including the presence and behaviour of others, has been predicted to mediate population-level processes even in the absence of cohesive grouping. However, we know little about how such effects may arise when the prey population lacks social structure beyond the spatiotemporal autocorrelation originating from the random movement of individuals. In this study, we built an individual-based model where predator avoidance behaviour could spread among randomly moving prey through the network of nearby observers. We qualitatively assessed how ISI use may affect prey population size when cue detection was associated with different probabilities and fitness costs, and characterised the structural properties of the emerging detection networks that would provide pathways for information spread in prey. We found that ISI use was among the most influential model parameters affecting prey abundance and increased equilibrium population sizes in most examined scenarios. Moreover, it could substantially contribute to population survival under high predation pressure, but this effect strongly depended on the level of predator detection ability. When prey exploited social cues in the presence of high predation risk, the observed detection networks consisted of a large number of connected components with small sizes and small ego networks; this resulted in efficient information spread among connected individuals in the detection networks. Our study provides hypothetical mechanisms about how temporary local densities may allow information diffusion about predation threats among conspecifics and facilitate population stability and persistence in non-grouping animals.
Significance statement
The exploitation of inadvertently produced social cues may not only modify individual behaviour but also fundamentally influence population dynamics and species interactions. Using an individual-based model, we investigated how the detection and spread of adaptive antipredator behaviour may cascade to changes in the demographic performance of randomly moving (i.e., non-grouping) prey. We found that social information use contributed to population stability and persistence by reducing predation-related per capita mortality and raising equilibrium population sizes when predator detection ability reached a sufficient level. We also showed that temporary detection networks had structural properties that allowed efficient information spread among prey under high predation pressure. Our work represents a general modelling approach that could be adapted to specific predator-prey systems and scrutinise how temporary local densities allow dynamic information diffusion about predation threats and facilitate population stability in non-grouping animals.
... Two such control methods include 1) the fungal pathogen Beauveria bassiana (Basalmo) Vuillemin [Hypocreales, Cordycipitaceae], which infects a host by penetrating the cuticle and invading the hemocoel, and 2) the spined soldier bug (Podisus maculiventris Say), which will consume all above-ground potato beetle life stages (Aldrich and Cantelo 1999). Spined soldier stink bugs produce many chemical compounds in their dorsal abdominal gland (Aldrich 1984), and they have been shown to elicit non-consumptive effects on potato beetles (Hermann and Thaler 2014, Kaplan et al. 2014, Hermann and Landis 2017. Non-consumptive effects occur when the mere presence of predators affects prey behavior, development or physiology. ...
The Sixth International Symposium on Biological Control of Arthropods, held virtually from British Columbia, Canada, continues the series of International Symposia on Biological Control of Arthropods, organized every four years. The history of the meetings is:
• First ISBCA, Hawaii, USA – January 2002
• Second ISBCA, Davos, Switzerland – September 2005
• Third ISBCA, Christchurch, New Zealand – February 2009
• Fourth ISBCA: Pucón, Chile – March 2013
• Fifth ISBCA: Langkawi, Malaysia – September 2017
The goal of these symposia is to create a forum where biological control researchers and practitioners can meet and exchange information, to promote discussions of up to date issues affecting biological control, particularly pertaining the use of parasitoids and predators as biological control agents. This includes all approaches to biological control: conservation, augmentation, and importation of natural enemy species for the control of arthropod targets, as well as other transversal issues related to its implementation.
To this end, 12 sessions have been organized in order to address the most relevant and current topics in the field of biological control of arthropods, delivered by invited speakers, contributed talks and poster presentations. To kick off ISBCA 2022, Dr. Martin Hill, Global President of the International Organization for Biological Control, presents an opening keynote talk on the current state of biological control. Some of the topics covered in ISBCA 2022 have remained as important issues since the first meeting, like the importance of biological control for managing invasive species, sustainable pest regulation in agricultural landscapes, the continuing challenges for biological control of forest pests, and the role of native vegetation in conservation biological control. But also, as new challenges and environmental concerns arise, some fresh topics have emerged. Among them are climate change and the disruption of biological control, stakeholder knowledge and perceptions of biological control, the use of native and exotic natural enemies for augmentative biological control, and functional diversity supporting biological control. For the first time, a workshop on biological control of ticks will be held. To show that biological control is a continuum linked to other disciplines, there will be a session on the science underpinning the successful use of pathogens in biological control. An important goal of the International Symposium on Biological Control of Arthropods is to promote early career researchers, and the first session Proceedings of ISBCA 6 – D.C. Weber, T.D. Gariepy, and W.R. Morrison III, eds. (2022) iii is organized to showcase the work of select individuals. The International Organization for Biological Control (IOBC) has sponsored these presentations. Another important goal of these meetings has been to be truly international, and this is why every conference so far has been organized in a different continent. This year we are excited in having achieved this goal despite the many world crises, by having participants from over 30 countries and all continents except Antarctica. We are particularly happy for the many works and participants from South America, a region that in the past has been poorly represented in these symposia. As a result, this meeting represents an opportunity for creating and expanding networks between researchers worldwide.
Thus we expect that, despite the virtual format, the 6th International Symposium on Biological Control of Arthropods would be an important milestone in keep moving forward the research and practice on biological control of arthropods, thereby helping to improve the sustainability of managed systems as well as aiding in the protection of biodiversity on the planet.
... Organisms have also evolved to assess and behaviorally respond to the mere risk of predation, 42 not just direct predator exposure (Hermann & Landis, 2017). Because predation results in 43 death, anti-predation behaviors, especially in non-social organisms, are usually innate rather 44 than learned, encoded in an organism's germ line and brain (Baker et al., 2001;Ren & Tao, 45 2020). ...
Ants are ubiquitous and consume insects at all life stages, presumably creating a strong selective pressure for ant avoidance behaviors across insects. The insect egg stage can be especially defenseless against predation given that eggs are usually immobile and unguarded, suggesting insect mothers may have evolved oviposition strategies to minimize the ant predation risk to their offspring. Given the lack of parental care in most insects, these oviposition strategies would likely be innate rather than learned, since insect mothers are not usually present to assess predation of their eggs. Here, we use the vinegar fly Drosophila melanogaster as a model system for examining parental defensive responses to ant presence. Flies usually lay eggs partially inserted into the food substrate, although some are laid on top of the food and a few are inserted deeply into the food. We found that exposure to ants significantly alters fly oviposition depth: the proportion of eggs on the food surface decreased while the proportion of buried eggs increased. Buried eggs survive ant foraging bouts better than surface eggs, showing that this oviposition depth behavior is adaptive. This induced behavior is conserved across the genus Drosophila and is dependent on the fly olfactory system: anosmic mutant flies fail to bury their eggs in the presence of ants, and ant odor extracts are sufficient to induce egg burying. By fractionating ant body washes and using GC-MS to identify fraction constituents, we identified the saturated, long-chain alcohol 1-octadecanol as the odorant flies use to sense ant presence. To further delineate the ant lineages to which flies respond, we exposed flies to the odors from numerous species of ants and other insects. Surprisingly, flies buried their eggs in response to the odors of nearly all hymenopterans tested, including hymenopteran groups that flies rarely interact with in nature like bees and paper wasps. Our data suggest that 1-octadecanol is a conserved and ancient hymenopteran odorant, and that drosophilids evolved a mechanism for sensing this odorant early in their evolution as a means of protecting their offspring from ant predation. This study sheds light on the ecology and mechanisms underlying a common biotic interaction in nature, that between insect parents and the ants that would consume their offspring.
... Behavioral traits of both predators and prey are of increasing interest, particularly the role these traits play in non-consumptive effects. Non-consumptive effects-in contrast to 'consumptive effects', which describe the capture and killing of prey by predators-encompass modified prey behavior, morphology, and/or physiology in response to perceived predation risk (Thaler et al. 2012;Hermann and Landis 2017). For instance, prey may reduce foraging activity or escape to different habitats to circumvent predators (Heithaus et al. 2009;Hermann and Thaler 2014), highlighting the challenge prey face in evading predation while also locating suitable food resources (Sih 1980). ...
Chemical cues play important roles in predator–prey interactions. Semiochemicals can aid predator foraging and alert prey organisms to the presence of predators. Previous work suggests that predator traits differentially influence prey behavior, however, empirical data on how prey organisms respond to chemical cues from predator species with different hunting strategies, and how foraging predators react to cues from potential competitors, is lacking. Furthermore, most research in this area has focused on aquatic and aboveground terrestrial systems, while interactions among belowground, soiling-dwelling organisms have received relatively little attention. Here, we assessed how chemical cues from three species of entomopathogenic nematodes (EPNs), each with a different foraging strategy, influenced herbivore (cucumber beetle) and natural enemy (EPN) foraging behavior. We predicted these cues could serve as chemical indicators of increased predation risk, prey availability, or competition. Our findings revealed that foraging cucumber beetle larvae avoided chemical cues from Heterorhabditis bacteriophora (active-foraging cruiser EPNs), but not Steinernema carpocapsae (ambusher EPNs) or Steinernema riobrave (intermediate-foraging EPNs). In contrast, foraging H. bacteriophora EPNs were attracted to cues produced by the two Steinernema species but not conspecific cues. Notably, the three EPN species produced distinct blends of olfactory cues, with only a few semi-conserved compounds across species. These results indicate that a belowground insect herbivore responds differently to chemical cues from different EPN species, with some EPN species avoiding prey detection. Moreover, the active-hunting EPNs were attracted to heterospecific cues, suggesting these cues indicate a greater probability of available prey, rather than strong interspecific competition.
... Within-generational and transgenerational plasticity of defense should be a successful adaptive defense strategy for SBPHs, given that rove beetle and other groups of predators such as predatory spiders are abundant all around the year in rice paddies. The higher mortality of SBPH nymphs when they experience predation risk, has been broadly addressed before 24,48,49 . Reduced food intake during risk periods may contribute to this poorer survival outcome, because insects are likely to alter their feeding behavior 50,51 , or shift from a high-risk host to a safer, but nutritionally inferior, one 52 , when they detect the presence of predators. ...
Predators can induce phenotypic plasticity in prey through selection driven by predation risk. However, defense plasticity is rarely reported in insects, let alone trans-generational plasticity, meaning the mechanisms underlying plasticity, how it impacts ecosystem evolution and how it might be exploited in pest control are poorly understood. Here we examine the morphological plasticity of small brown planthoppers (SBPHs), Laodelphax striatellus , elicited by caged predators, Paederus fuscipes in the parent or F1 generation and reveal the risk cues mediating these effects. We also uncover the survival outcomes in SBPHs with predator-induced defensive morphological traits by examining their survival probability and behavioral plasticity. Results showed that caged predators or predator odor cue gave rise to a higher proportion of long-winged, female SBPHs in the parent and F1 generations, but the proportion of males and their wing length were unaffected. The visual cue from predators elicited weaker effects. Surprisingly, we discovered these long-winged forms suffered a lower predation rate when attacked by P. fuscipes, owing to an enhanced agility level. Our results suggest the within- and trans-generational plasticity of induced defenses may cause profound effects on SBPH population dynamics and prey-predator interaction. Understanding this interaction and its underlying mechanisms illuminates important aspects of ecosystem evolution and helps predict pest dispersal or migration, which in turn may be exploited for pest control.
... As insect preys face diverse predator assemblages, they must detect and respond to spatially and temporally variable predation risk. Insects can identify visual, volatile, and contact cues from predators when selecting feeding or oviposition sites, and respond to such cues by altering their behavior, physiology, or morphology in ways that reduce mortality and/or ensure the safety of offspring (Ninkovic et al. 2013;Hermann and Thaler 2014;Beleznai et al. 2015;Hermann and Landis 2017;Culshaw-Maurer et al. 2020). However, changes in insect behavior in response to predators may also affect diet quality, feeding duration, and fecundity (Preisser et al. 2007;Preisser and Bolnick 2008;Jones and Dornhaus 2011). ...
Herbivores assess predation risk in their environment by identifying visual, chemical, and tactile predator cues. Detection of predator cues can induce risk-avoidance behaviors in herbivores that affect feeding, dispersal, and host selection in ways that minimize mortality and reproductive costs. For herbivores that transmit plant pathogens, including many aphids, changes in herbivore behavior in response to predator cues may also affect pathogen spread. However, few studies have assessed how aphid behavioral responses to different types of predator cues affect pathogen transmission. Here, we conducted greenhouse experiments to assess whether responses of pea aphids (Acyrthosiphon pisum) to predation risk and alarm pheromone (E-β-Farnesene), an aphid alarm signal released in response to predation risk, affected transmission of Pea enation mosaic virus (PEMV). We exposed A. pisum individuals to risk cues, and quantified viral titer in aphids and pea (Pisum sativum) host plants across several time periods. We also assessed how A. pisum responses to risk cues affected aphid nutrition, reproduction, and host selection. We show that exposure to predator cues and alarm pheromone significantly reduced PEMV acquisition and inoculation. Although vectors avoided hosts with predator cues, predator cues did not alter vector reproduction or reduce nutrient acquisition. Overall, these results suggest that non-consumptive effects of predators may indirectly decrease the spread of plant pathogens by altering vector behavior in ways that reduce vector competence and pathogen transmission efficiency.
... Indeed, chemical cues are important mediators of non-consumptive effects (NCEs) in predator-prey relationships (Ferrari et al., 2010;Hill and Weissburg, 2013). Response to predator cues leads to alterations in behavior and physiology that reduce an individual's risk of predation (Weissburg and Beauvais, 2015;Hermann and Landis, 2017). Relatively less is understood about the role of chemical cues in mediating NCEs of parasites and parasite-host interactions (Fink, 2007;Saha et al., 2019). ...
Chemical communication within an aquatic environment creates an intricate signaling web that provides species with information about their surroundings. Signaling molecules, like oxylipins, mediate a multitude of interactions between free-living members of a community including non-consumptive effects by predators. Parasites are another source of signaling molecules in aquatic communities and contribute directly by synthesizing them or indirectly by manipulating host chemical cues. If chemical cues of infected hosts are altered, then non-consumptive interactions between other members of the community may also be affected. Different cues from infected hosts may alter behaviors in other individuals related to foraging, competition, and defense priming. Here, we discuss how parasites could modify host chemical cues, which may have far reaching consequences for other community members and the ecosystem. We discuss how the modification of signaling molecules by parasites may also represent a mechanism for parasite-modified behavior within some systems and provide a mechanism for non-consumptive effects of parasites. Further, we propose a host-parasite system that could be used to investigate some key, unanswered questions regarding the relationship between chemical cues, parasite-modified behavior, and non-consumptive effects. We explain how trematode-gastropod systems can be used to test whether there are alterations in the diversity and amounts of signaling molecules available, and if habitat use, immune function, and behavior of other individuals and species are affected. Finally, we argue that changes to pathway crosstalk by parasites within communities may have broad ecological implications.
... In d, e, and f, the significant differences were determined using the Student's t test (*p ≤ 0.05, and ***p ≤ 0.0001) lepidopteran mothers, S. litura mothers also know what is best for the early instars (Jaenike 1978;Thompson and Pellmyr 1991;Valladares and Lawton 1991). Since the selection of castor was not an oviposition mistake, and the host switch was to compensate for such mistake, we analyzed the role of natural enemies as their consumptive and non-consumptive pressures are known to influence the behavior and performance of the prey species and cause migration (Hermann and Landis 2017;Matassa and Trussell 2011;Orrock et al. 2011;Singer 2016;Xiong et al. 2015). Although the natural enemy abundance on eggplant was slightly higher than castor, S. litura larvae migrated to the eggplants. ...
Trap crops are used for pulling the pest load from the main crops toward themselves. Here, we report a switching by a polyphagous pest, Spodoptera litura, from trap crop castor to main crop eggplant during its mid-larval development. In the eggplant–castor mixed field, adults oviposit exclusively on castor. However, 3rd and 4th instar castor-grown larvae migrate to eggplants. Host choice assays for adults and larvae conducted in the controlled environment and the nutritional indices of castor and eggplant-feeding larvae revealed that the natural enemies did not influence the host switch. The host switch was rather associated with larvae’s enhanced digestion and metabolism. It shortened the development time and increased the eclosion success on eggplant. Mother-selected castor is suitable for the early instars and eggplant is for the later instars, indicating that the host switching was not because of the mother’s erroneous host choice but has evolved as an advantageous behavior. S. litura’s ability to switch hosts in the same ontogenic phase and reduce the generation time can contribute to an additional generation within a cropping season and endanger the critical growth stage of fruiting. Our findings support the ‘mother knows the best’ concept and annex that the larvae can also possess the ability to know the best. Such ability in different ontogenic stages can be fundamental to the exceptional adaptability of species like S. litura.
... Ng (2018) suggested that the mixed responses of herbivores and predators to plant species composition or vegetation structure include that a high proportion of herbivorous beetles may be attracted to plant species that are largely limited to habitat edges, e.g., Blue cranesbill (Erodium crinitum, Geraniaceae), tumbleweed (Salsola australis, Amaranthaceae) and wild mustard (Sisymbrium sp., Brassicaceae). Herbivores may allocate more time to foraging in complex habitats because they provide protection from predators through consumptive and nonconsumptive effects (Langellotto and Denno 2004, Blubaugh et al. 2017, Hermann and Landis 2017. ...
Agricultural production is increasingly viewed as more than a source of food, feed, fiber and fuel, but also as a system of interdependent biotic and abiotic components that interact to produce ecosystem services and disservices. Weeds and insects are commonly viewed as non-desirable components of agroecosystems that should be managed. However, weeds can also provide benefits to cropping systems, such as providing resources and habitat to pollinators and other beneficial arthropods. This review on weed–insect interactions in annual cropping systems focuses on functional interactions within the context of regulating and supporting ecosystem services and disservices. Regulating services are those that act as regulators of the environment, such as weed–insect interactions that contribute to the regulating services of pollination and biological control, but also contribute to the disservices of crop and cover crop seed predation, and maintenance of insect pests and insect-transmitted phytopathogens. Supporting services include habitat and biodiversity that are necessary for the production and maintenance of the other types of ecosystem services. Here we review the impacts of weed–insect interactions as a component of biodiversity. We conclude by identifying some knowledge gaps that hinder our understanding of trade-offs when seeking to improve net positive ecosystem services in annual cropping systems.
... Moreover, basal prey organisms benefit indirectly from the suppression of feeding by intermediate predators in the presence of top predators through a process known as traitmediated indirect interactions (TMIIs) [3,5,6]. Non-consumptive effects (NCEs) arise from non-lethal changes in the biology or behavior of intermediate predators that lead to their reduced fitness [13,15,16]. For example, reduced feeding due to predator avoidance reduces the energy available for growth and reproduction [14,17]. ...
How interactions among multiple predators affect the stability of trophic cascades is a topic of special ecological interest. To examine factors affecting the stability of the classic tri-trophic oyster reef cascade within a different context, configurations of three predators, including the Gulf toadfish, Gulf stone crab, and oystershell mud crab, were manipulated together with either oyster shell or limestone gravel substrate within a multiple predator effects (MPE) experiment. Additionally, a complimentary set of trait-mediated-indirect interaction (TMII) experiments examined the inhibition of oyster consumption relative to mud-crab size and top predator identity in the absence of other cues and factors. The classic tri-trophic cascade formed by the toadfish-mud crab-oyster configuration was potentially weakened by several interactions within the MPE experiment. Consumption of oysters and mud crabs by the intra-guild stone crab was undeterred by the presence of toadfish. Although mud crab feeding was inhibited in the presence of both toadfish and stone crabs, estimated non-consumptive effects (NCEs) were weaker for stone crabs in the MPE experiment. Consequently, the total effect was destabilizing when all three predator species were together. Inhibition of mud crab feeding was inversely related to direct predation on mud crabs within the MPE experiment. Complimentary TMII experiments revealed greater inhibition of mud crab feeding in response to stone crabs under sparse conditions. TMII experiments also implied that inhibition of mud crab feeding could have largely accounted for NCEs relative to oysters within the MPE experiment , as opposed to interference by other mud crabs or top predators. An inverse relationship between mud crab size and NCE strength in the TMII experiment disclosed another potentially destabilizing influence on the tri-trophic-cascade. Finally, although habitat complexity generally dampened the consumption of oysters across MPE treatments, complex habitat promoted mud crab feeding in the presence of toadfish alone. This study underscores how ecological interactions can mediate trophic cascades and provides some additional insights into the trophic dynamics of oyster reefs for further testing under natural conditions.
... In the wake of recent conservation campaigns worldwide, there has been increased attention to mitigating human-wildlife conflicts with non-lethal tools (Van Eeden et al., 2018), including deterrents and aversive conditioning (Schakner & Blumstein, 2013). Such tools may also be used manage rodents and insects that are agricultural pests (Hermann & Landis, 2017;Krijger et al., 2017) or carry diseases (Staats, Agosta, & Vonesh, 2016;Moll et al., 2020). Managers may use similar tools to reduce behaviors that put animals at risk, such as crossing roads (Proppe et al., 2016), or behaviors that compromise other ecological and natural resource management goals, like foraging on seedlings in forestry or restoration areas (Beringer et al., 1994). ...
Research on the ecology of fear has highlighted the importance of perceived risk from predators and humans in shaping animal behavior and physiology, with potential demographic and ecosystem-wide consequences. Despite recent conceptual advances and potential management implications of the ecology of fear, theory and conservation practices have rarely been linked. Many challenges in animal conservation may be alleviated by actively harnessing or compensating for risk perception and risk avoidance behavior in wild animal populations. Integration of the ecology of fear into conservation and management practice can contribute to the recovery of threatened populations, human–wildlife conflict mitigation, invasive species management, maintenance of sustainable harvest and species reintroduction plans. Here, we present an applied framework that links conservation interventions to desired outcomes by manipulating ecology of fear dynamics. We discuss how to reduce or amplify fear in wild animals by manipulating habitat structure, sensory stimuli, animal experience (previous exposure to risk) and food safety trade-offs to achieve management objectives. Changing the optimal decision-making of individuals in managed populations can then further conservation goals by shaping the spatiotemporal distribution of animals, changing predation rates and altering risk effects that scale up to demographic consequences. We also outline future directions for applied research on fear ecology that will better inform conservation practices. Our framework can help scientists and practitioners anticipate and mitigate unintended consequences of management decisions, and highlight new levers for multi-species conservation strategies that promote human–wildlife coexistence.
... Examples of such nonconsumptive effects are the changes in behaviour to reduce the risk of being attacked, which have been largely documented in prey exposed to predators. Such changes in behaviour have positive effects for the prey, which is thus able to escape from predation, but are associated with important fitness costs (Hermann & Landis, 2017). In parasite-host systems, although less studied, the avoidance of parasites has also been associated with important fitness costs that ultimately affect the survival and fecundity of the hosts (Buck et al., 2018;Horn & Luong, 2018). ...
This study aimed to evaluate the effects of egg dormancy times on susceptibility of larvae of the floodwater mosquito Aedes albifasciatus (Diptera: Culicidae) to parasitism by their natural enemy Strelkovimermis spiculatus (Nematoda: Mermithidae) and on their life history traits. Aedes albifasciatus eggs stored for 2, 4, 6, 8 and 10 months were hatched, and the larvae either exposed to S. spiculatus (treatment group) or not exposed (control group). Egg dormancy time had a negative effect on the retention of parasites, but no effect on the prevalence and intensity of parasitism or the melanization of nematodes. The survival to adulthood of control individuals decreased as dormancy time increased, whereas that of exposed individuals that remained uninfected was constant and low. A trend towards increasing development times with longer dormancy times was detected in the control group, but not in the exposed noninfected group. The results suggest nonconsumptive effects of parasites in exposed but not infected larvae from eggs with short dormancy times. In contrast, the relatively low fitness of larvae from eggs with long dormancy times regardless of their contact with the nematodes may be the result of the nutritional deprivation during the egg stage. The effect of dorma ncy time of Aedes albifasciatus eggs on the host‐parasite interaction with the nematode Strelkovimermis spiculatus was assessed for the first time. The increased egg dormancy time affects the survival and immature development time of Aedes albifasciatus, but not the susceptibility to infection by Strelkovimermis spiculatus. The low survival of larvae exposed to the nematode that avoided infection suggest nonconsumptive effects of the parasites, especially in larvae from eggs with short dormancy times.
... While the majority of NCE studies are completed on short time scales (Preisser et al., 2009;Hermann & Landis, 2017), many mechanisms operating over longer time scales have the potential to alter the strength of NCEs. The predation risk allocation hypothesis states that prey must balance foraging needs and anti-predation measures depending on the temporal changes in perceived risk (Lima & Bednekoff, 1999). ...
• The influence of predator cues on the behaviour of prey is well supported in the literature; however, a clear understanding of how predator cues affect prey in variable environmental conditions and over longer time scales is needed to better understand the underlying mechanisms. Here, we measure how predator odors affect herbivore colonization, abundance, oviposition, and plant damage across two growing seasons.
• The study system consisted of Leptinotarsa decemlineata (Colorado potato beetle) as prey, and the aggregation pheromone of live Podisus maculiventris (spined soldier bug) as the predator cue in a potato field.
• In 2016, the amount of feeding damage by early beetle colonists was lower in predator odor‐treated plots, reducing plant damage by 22%. Larval abundance was also reduced in treated plots in 2016. Beetle abundance and damage in 2017 was similar in the treatment and control plots. Two mechanisms were investigated to better understand why prey response to the predator odor treatment weakened over the first season, including changes in predator odor cue strength and prey habituation. Predator odor cue strength emerged as a likely explanation, as dispensers, which released a synthetic predator pheromone over the entire season, reduced the probability of finding damage more consistently than the live predator treatment.
• These results suggest that temporal patterns of predator cue release and strength may drive prey response across the season, underscoring the importance of cue release‐rate and consistency in both species interactions and for the future application of modifying insect behaviour using non‐consumptive effects in agricultural systems.
... Non-consumptive effects are costly defensive strategies induced in prey by predators, leading to decreased survival (Siepielski et al. 2014) or fecundity (Peckarsky et al. 1993), as well as a change in growth or development time (Xiong et al. 2015), or change in activity (Kaplan et al. 2014). The importance of non-consumptive effects have been well established in terrestrial arthropods, where prey often rely on plants as a food source (reviewed in Buchanan et al. 2017;Hermann and Landis 2017). Thus, in these systems both predators (top-down) and host plant quality (bottom-up) interact to impact herbivore populations (Price et al. 1980;Poelman et al. 2008). ...
Predators impact prey populations through both consumptive and non-consumptive effects, such as behavioral and physiological changes by prey in response to a predation threat. Additionally, various top-down (e.g. predator characteristics) and bottom-up factors (e.g. plant nutrients) may impact non-consumptive effects, yet little is understood about how these interact. We studied how host-plant choice, leaf consumption, and growth of an herbivore, Pieris rapae, were impacted by different levels of plant nitrogen (N) and two predator species representing varying degrees of threat, Hippodamia convergens (predator of early-instars) and Podisus maculiventris (predator of all-instars). We found that P. rapae adults and larvae made similar choices about bottom-up and top-down factors when threatened by two different predator species. Adults and larvae preferred high N plants when threatened by H. convergens, but plant N did not influence their host plant choice when threatened by P. maculiventris. Additionally, larvae consumed more leaf tissue and grew larger when threatened by H. convergens, but leaf tissue consumption and larval growth did not change under threat by P. maculiventris, suggesting that larvae may change their behavior if they are able to quickly outgrow life stages vulnerable to predation. These results indicate that top-down factors such as predator identity may determine how P. rapae modulate their responses to bottom-up factors such as host plant quality when utilizing anti-predator behaviors.
... However, as in vertebrates (Harris and Carr 2016), activating anti-predator responses is energetically costly in insects (Buchanan et al. 2017;Hermann and Landis 2017). Exposure to a live predator results in a reduction in whole body glycogen in 3rd instar M. sexta (Thaler et al. 2012). ...
When animals are faced with a life-threatening challenge, they mount an organism-wide response (i.e. Plan A). For example, both the stress response (i.e. fight-or-flight) and the immune response recruit molecular resources from other body tissues, and induce physiological changes that optimize the body for defense. However, pathogens and predators often co-occur. Animals that can optimize responses for a dual challenge, i.e. simultaneous predator and pathogen attacks, will have a selective advantage. Responses to a combined predator and pathogen attack have not been well studied, but this paper summarizes the existing literature in insects. The response to dual challenges (i.e. Plan B) results in a suite of physiological changes that are different from either the stress response or the immune response, and is not a simple summation of the two. It is also not a straight-forward trade-off of one response against the other. The response to a dual challenge (i.e. Plan B) appears to resolve physiological trade-offs between the stress and immune responses, and reconfigures both responses to provide the best overall defense. However, the dual response appears to be more costly than either response occurring singly, resulting in greater damage from oxidative stress, reduced growth rate, and increased mortality.
... Predator preference, satiation and prey switching are the factors thought to be responsible for changes in the strength and directionality of consumptive effects of predation on the indirect interactions between prey (Abrams & Matsuda, 1996;Holt & Bonsall, 2017). Another form of indirect interaction between predators and prey relates to non-consumptive or trait-mediated effects in which prey respond to the presence of a predator through shifts in host plant preference, within-plant distribution, predator-avoidance behaviour and/or reductions in feeding and reproduction (Preisser et al., 2005;Buchanan et al., 2017;Hermann & Landis, 2017). There is often a trade-off between risk of predation and prey fitness associated with the non-consumptive effects of predation, caused by prey moving to plant species or parts of a plant that have lower nutritive value. ...
1. Generalist predators are important contributors to reliable conservation biological control. Indirect interactions between prey species that share a common generalist predator can influence both community dynamics and the efficacy of biological control. 2. Laboratory cage experiments investigated the impact of the combined consumptive and non‐consumptive effects of predation by adult Hippodamia convergens as a shared predator on the population growth and relative abundance of Acyrthosiphon pisum and Aphis gossypii as prey species. Predation pressure and prey density were varied. 3. At low predation pressure the indirect interaction between aphid species was asymmetrical with a proportionally greater negative impact of predation on A. gossypii than on A. pisum. At intermediate predation pressure, the indirect interaction became symmetrical. At high predation pressure and higher levels of prey density, it was asymmetrical with greater negative impact on A. pisum, often driven to local extinction while A. gossypii populations persisted. 4. A linear mixed‐effects model including early population growth of both aphid species and predation pressure explained 96% and 92% of the variation in the population growth of A. pisum and A. gossypii, respectively, over an 8‐day period. The overall effect of shared predation on the indirect interaction between the two aphid species is best described as apparent commensalism, where A. pisum benefited from early population growth of A. gossypii, while A. gossypii was unaffected by early population growth of A. pisum. Considering these indirect interactions is important for conservation biological control efforts to be successful. As Hippodamia convergens shows no preference between Acyrthosiphon pisum and Aphis gossypii, shifts in indirect interactions between prey are more likely. Evidence is provided for a proof of concept that differing predation pressure and prey density can have both symmetrical and asymmetrical effects that shift the relative population abundance in a two‐prey system. Mixed models of the predation pressure experiment show that A. pisum benefits from greater early population growth of A. gossypii, indicating overall apparent commensalism between the two prey species.
... This includes the use of the entomopathogenic fungus Beauveria bassiana (Basalmo) Vuillemin, which infects insects by penetrating the cuticle and invading the hemocoel, and the spined soldier bug (Podisus maculiventris Say), which readily consumes all aboveground beetle life stages Cantelo 1999, Hilbeck andKennedy 1996). These stink bugs produce a suite of chemical compounds in their dorsal abdominal glands that they use as an aggregation pheromone (Aldrich et al., 1984, Sant'ana et al. 1999, and they can elicit a suite of non-consumptive effects on potato beetles (Hermann and Thaler, 2014, Kaplan et al. 2014, Hermann and Landis, 2017. Non-consumptive effects are effects of predators on prey traits such as behavior, development or physiology that occur when the prey detect, but are not eaten by the predator. ...
Lethal predators and pathogens can reduce the size of pest populations and help regulate crop-damaging herbivores. Additionally, predators like the spined soldier bug (Podisus maculiventris) can elicit non-consumptive effects in herbivores such as the Colorado potato beetle (Leptinotarsa decemlineata), causing changes in prey behavior, physiology and life history. While it is known that lethal predators and pathogens interact, there is little known about the interaction of predator-induced non-consumptive effects and pathogens on their shared hosts. Using the spined soldier bug, which is known to elicit non-consumptive effects on potato beetles (e.g. reduced feeding), we studied the interaction of predator-induced non-consumptive effects and the fungal pathogen Beauveria bassiana on the survival of Colorado potato beetle larvae. In laboratory microcosms we found a 16–50% increase in survival of fungus-treated beetles held with non-lethal male stink bugs. We also studied the predator-fungus interaction on jasmonic acid-treated plants to assess whether elevated levels of host plant defenses made larvae more susceptible to fungal infection. Beetles’ susceptibility to fungal infection did not change when provided jasmonic-acid treated foliage as food. Finally, we determined that two volatile compounds (E-2-hexenal and alpha-terpineol), produced as part of the bugs’ aggregation pheromone, reduced conidial germination, resulting in higher levels of beetle survival. Our findings suggest that stink bug odors protect prey against fungal pathogens.
... http://dx.doi.org/10.1101/2019.12.27.889634 doi: bioRxiv preprint first posted online Dec. 28, 2019; 5 predator defences by insects with extreme phenotypic plasticity, such as aphids, have not been 141 sufficiently investigated and understood as yet. 142 Brevity versus longevity of non-consumptive effects 143 The evidence for the wide-spread impact of fear of predation is mounting across a vast 144 array of taxa (Preisser et al., 2005;Hermann and Landis, 2017). However, the current 145 understanding of the role of the duration of risk exposure is meagre, particularly in respect to the 146 influence of non-consumptive effects on phloem-feeding insect biology, but see (Van Dievel et this preprint (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in (Ninkovic et al., 2013). ...
Non-consumptive effect of predation is a well-researched subject of which certain non-consumptive and predator-mimetic facets are yet to be investigated in plant-parasite systems
One clone of the green peach aphid Myzus persicae (Sulzer), raised on a model crop Brassica oleracea (L.), was exposed to different regimes of risks associated with ladybird Coccinella septempunctata (L.). This encompassed consumption, consumption alternated by non-consumptive effects, isolated predators, dead predator, predator dummy, as well as dummy, plants or soil cued with predator-borne suspension, and predator removal (exposure to plants previously visited and marked by a predator).
Over time, the respective risk regimes variably negatively impacted the prey population; the corpses, cued plants and dummies had considerable persistent negative effects on aphid reproductive success, contrary to the observation under predator removal. By the end of the experiment, polyphenism (winged morph production) also differed and was animated under the presence of a starved isolated predator; but faded when a predator corpse was present; and vanished under the dummy. Our findings, in this model aphid-crop system, contribute to the rapidly developing area of the ecology of fear, as we provide insights and novel means for aphid management that merit further examination across different eco-agricultural contexts.
... However, very little is known about vibrations perceived by beetle larvae inside the seed. Non-consumptive effects of predators and parasitoids have been shown to have important consequences on herbivore population dynamics 5,7,11,[67][68][69] . For instance, Thaler and Griffin 70 showed that the negative impact of a predatory stinkbug (Podisus maculiventris) on the feeding activity of an herbivorous insect prey (Manduca sexta) was approximately the same when they removed the predator's rostra, preventing them from killing their prey. ...
The interaction between the seed beetle Zabrotes subfasciatus and its parasitoid Stenocorse bruchivora, was investigated on seeds of two populations of wild lima bean, Phaseolus lunatus. By manipulating the number of beetle larvae per seed and the presence of parasitoids, we determined how factors related to beetle larvae density, the seed in which they feed and the parasitoid, may interact and affect host and parasitoid survival. Results showed that an increase in larval beetle density had a negative impact on beetle performance. This effect cascaded up to parasitoids, high larval density strongly reduced parasitoid emergence. Also, parasitoid presence resulted in faster beetle development and lower female weight. An interactive effect between larval host density and parasitoid presence affected the number of insects that emerged from the seeds. Beetle performance was better in the bean population with the largest seeds, while parasitoid emergence was the lowest in these seeds. This study shows that the impact of parasitoids on seed beetles is contingent on the interaction between density-mediated (direct mortality) and trait-mediated (e.g. non-consumptive) effects. Indirect trait-mediated effects of natural enemies are likely prevalent across insect communities, understanding their role in driving host-parasitoid interactions can have important implications for biological control.
... Summary statistics of the LMER models used to estimate marginal means and confidence intervals are available in Table 1 62,63 . Recent studies have shown that such behavioral effects are ubiquitous in biocontrol systems and potentially affect pest suppression [64][65][66][67][68] , as demonstrated herein. In complex landscapes, some of the mechanisms of reducing niche overlap (e.g., spatial separation or the availability of alternative preys) Figure 6. ...
Biological pest control by natural enemies is an important component of sustainable crop production. Among biological control approaches, natural enemy augmentation is an effective alternative when naturally occurring enemies are not sufficiently abundant or effective. However, it remains unknown whether the effectiveness of augmentative biocontrol varies along gradients of landscape composition, and how the interactions with resident enemies may modulate the collective impact on pest suppression. By combining field and lab experiments, we evaluated how landscape composition influenced the effectiveness of predator augmentation, and the consequences on pest abundance, plant damage, and crop biomass. We show for the first time that the effectiveness of predator augmentation is landscape-dependent. In complex landscapes, with less cropland area, predator augmentation increased predation rates, reduced pest abundance and plant damage, and increased crop biomass. By contrast, predator releases in simple landscapes had a negative effect on pest control, increasing plant damage and reducing crop biomass. Results from the lab experiment further suggested that landscape simplification can lead to greater interference among predators, causing a decrease in predator foraging efficiency. Our results indicate that landscape composition influence the effectiveness of augmentative biocontrol by modulating interactions between the introduced predators and the local enemy community.
... This tripartite complex, comprising EPNs, their bacterial symbionts and the infected host, produces a variety of metabolites with different roles in EPN ecology, development and reproduction (Hu, Li, & Webster, 1999;Hu & Webster, 2000;Kaplan et al., 2012;Lu et al., 2017). Based on studies from above-ground systems, it is clear that many prey species avoid chemical cues from potential predators (Hermann & Landis, 2017;Kats & Dill, 1998). Female insects also frequently use chemical cues to select suitable oviposition sites and to avoid plant defences, competition or elevated predation risk for their offspring (Kariyat et al., 2013;De Moraes, Mescher, & Tumlinson, 2001). ...
Chemical cues are essential for many ecological interactions. Previous studies of chemically mediated multitrophic interactions have typically focused on responses to cues from plants or herbivores above‐ground. It is increasingly clear, however, that below‐ground cues and those produced by organisms at higher trophic levels also have ecological importance. Prey animals often avoid predator odours to improve survival, and previous research has documented enhanced plant resistance following contact with below‐ground natural enemies, though the ecological basis was unknown. Here, we investigated plant and insect responses to chemical cues from below‐ground natural enemies and explored the ecological significance of these cues for multitrophic interactions. More specifically, we examined the influence of odours emitted by entomopathogenic nematodes (EPNs), a natural enemy of insect herbivores, on the performance and behaviour of their insect prey and the defence responses of nearby plants. Our findings revealed that EPN‐infected insect cadavers emit a characteristic blend of volatile compounds with bioactivity in plants and insects. EPN chemical cues influenced both performance and preference of a specialist herbivore, Colorado potato beetle (CPB, Leptinotarsa decemlineata), feeding on its host plant, potato (Solanum tuberosum). CPB larvae consumed less leaf tissue and gained less mass feeding on plants exposed to EPN cues compared to control plants. Female CPBs laid fewer eggs on plants with EPN cues than on controls, indicating deterrence by EPN cues or EPN‐altered plant defences. Plant defences were enhanced by exposure to live EPNs or EPN chemical cues. Potato plants exposed to EPN infective juveniles induced higher amounts of the defence hormone salicylic acid (SA) and had higher expression of the pathogenisis‐related gene PR‐1(PR4) in foliar tissue. Exposing plants to EPN cues primed induction of SA and jasmonic acid in response to feeding damage by CPB larvae. These findings suggest that herbivores avoid cues from their EPN natural enemies and plants respond to the beneficial nematodes by enhancing systemic defences that reduce herbivore performance. This work has important implications for the chemical ecology of tritrophic interactions as we report that the third trophic level can play direct and indirect roles in plant defence. A plain language summary is available for this article. Plain Language Summary
Coastal elasmobranchs tend to be upper-level predators, which may exert top-down impacts on the systems they inhabit; but there remains much to learn about their trophic ecology. In this chapter, we update our knowledge on the trophic interactions of coastal elasmobranchs as prey, predators, and competitors. We also explore factors that affect these relationships and elasmobranch interactions within key coastal habitats.
Alternative environmentally friendly methods for pest control are in high demand because of the environmental impacts of pesticides. Notably, predator‐released kairomone is a natural compound released by natural enemies, which mediates non‐consumptive effects between natural enemies and prey. However, this novel pest control agent is underutilized relative to pesticides and natural enemies. Additionally, the effects of spraying predator kairomone on the number and diversity of arthropods in fields and whether this method is environmental‐friendly are poorly understood. In the present study, a predator kairomone, rove beetle (Paederus fuscipes Curtis) abdominal gland secretion (AGS), was sprayed in rice fields to investigate whether AGS can suppress pest populations or will affect the fields’ arthropod communities. After AGS spraying, the abundance of arthropods decreased throughout the first 12‐d period, including arthropod pests such as hemipterans (small brown planthopper, Laodelphax striatellus (Fallén), brown planthopper, Nilaparvata lugens (Stål), white‐backed planthopper, Sogatella furcifera (Horváth), and leafhoppers), and lepidopterans (rice leaf folder, Cnaphalocrocis medinalis Guenée). The abundance of arthropod predators was not affected, except for predatory spiders, which decreased, and rove beetles (P. fuscipes), which increased. In the terms of arthropod diversity, neither pests nor their natural enemies were changed by AGS application. This work highlights that predator kairomone can temporarily suppress pest populations in fields but has no adverse effects on arthropod diversity; thus, this approach is environmentally friendly and can be used in real‐world applications. Broadly, present studies suggest that the application of predator kairomone may have synergistic or cumulative effects on pest suppression.
Insects, like other animals, have evolved defense responses to protect against predators, pathogens and poisons (i.e. toxins). This paper provides evidence that these three defense responses (i.e. fight-or-flight, immune and detoxification responses) function together as part of an Integrated Defense System (IDS) in insects. The defense responses against predators, pathogens and poisons are deeply intertwined. They share organs, resources and signaling molecules. By connecting defense responses into an Integrated Defense System, animals gain flexibility and resilience. Resources can be redirected across fight-or-flight, immune and detoxification defenses to optimize an individual's response to the current challenges facing it. At the same time, the IDS reconfigures defense responses that are losing access to resources, allowing them to maintain as much function as possible despite decreased resource availability. An IDS perspective provides an adaptive explanation for paradoxical phenomena such as stress-induced immunosuppression, and the observation that exposure to a single challenge typically leads to an increase in the expression of genes for all 3 defense responses. Further exploration of the IDS will require more studies examining how defense responses to a range of stressors are interconnected in a variety of species. Such studies should target pollinators and agricultural pests. These studies will be critical for predicting how insects will respond to multiple stressors, such as simultaneous anthropogenic threats, e.g. climate change and pesticides.
1. Differences in hatching dates can shape intraspecific interactions through size-mediated priority effects (SMPE), a phenomenon where bigger, early hatched individuals gain advantage over smaller, late hatched ones. While SMPE may be important for population dynamics, to what extent and how these are affected by key environmental factors such as warming and predation risk imposed by top predators remains unclear.
2. In a laboratory experiment, we studied effects of warming (low and high temperature) and predation risk (presence and absence of predator cues of perch) on SMPE in life history and physiological traits in the cannibalistic damselfly Ischnura elegans. We induced SMPE by manipulating hatching dates, thereby creating four groups: non-mixed phenology early (E) and late (L) hatchers, and mixed phenology early (E+L) and late (L+E) hatchers.
3. We found strong SMPE for survival and emergence success, with the highest values in E+L larvae and the lowest values in L+E larvae. Neither temperature nor predator cues affected SMPE for these two life history traits. The other life history traits (development rate and mass at emergence) did not show SMPE, but were affected by temperature and predator cues.
4. SMPE was found for protein content, but only in the high temperature treatment. The other physiological traits (immune function measured as phenoloxidase activity and fat content) showed fixed expressions across treatments, indicating decoupling between physiology and life history.
5. The results underline that SMPEs are trait-dependent, and only weakly affected by temperature and predation risk.
Predator non-consumptive effects (NCEs) have been well studied in many ecosystems and NCEs can alter the behavior, morphology and life history of prey, producing strong trait-mediated indirect effects (TMIEs) on host plants. However, studies involving the application of NCEs to control pests in the field, and instances of combined laboratory bioassay and field practice are rare. Here, we examine the development, reproduction and behavior of small brown planthoppers, Laodelphax striatellus (Fallén), when exposed to predator cues from caged predators (Paederus fuscipes Curtis), or predator body extracts (in solvents with different polarities) in the laboratory. Field foliage sprays of these extracts were also used to test their effects on the L. striatellus population and rice plant biomass. Nymph development and egg hatch rate in L. striatellus were not influenced, but adult longevity was shorter, and fecundity and weight gain were lower, when nymphs were exposed to the predator cues. Adults exposed to predator cues also gained less weight and laid fewer eggs. The poorer developmental and reproductive performances might result from lower activity levels observed in threatened L. striatellus. The field foliage sprays of predator cues decreased L. striatellus abundance and increased rice plant biomass, suggesting their possible application for pest control. Predator cues extracted using chloroform increased stronger NCEs and TMIEs, indicating their non-polar characteristics. Our studies advance the understanding of how NCEs shape the life history and behavior of L. striatellus and improve rice growth, laying new foundations for future research on novel pest control materials and methods.
The impact of predatory or parasitic natural enemies on their pest prey or hosts arises not only through consumption but also through non-consumptive effects. Multiple studies have investigated the impacts of non-consumptive effects from predators on the behaviour, development and metabolism of invertebrate pests. However, the non-consumptive effects from parasitoids on their insect hosts remain less well understood. Here, we investigated the non-consumptive effects of the parasitoid Encarsia formosa on the fecundity, longevity and metabolism of the whitefly Bemisia tabaci. Results showed that both the fecundity and longevity of whitefly females were significantly reduced when the whiteflies were threatened by Encarsia parasitoids during their nymphal stages. In addition, we tested three costly and potential physiological correlates that may contribute to the fecundity and longevity variation of B. tabaci under the non-consumptive effects: the relative expression level of vitellogenin and its receptor genes (Vg and Vgr), relative expression level of stress proteins (Hsp70 and Hsp90) and the activities of the antioxidant enzymes superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD). When B. tabaci 4th instar nymphs were threatened for 24 h by E. formosa the relative expression levels of Vg and Vgr were reduced, whereas Hsp70 and Hsp90 were significantly increased. SOD and CAT activities were distinctly up-regulated while POD activity was down-regulated. We propose that, in order to counteract the negative effects of non-consumption, whitefly nymphs need to adjust their performance by changing the expression of related metabolic genes in an energetic cost way, thus reducing the fecundity and longevity of female adults.
en Predators alter ecological communities by inducing changes in prey abundance and phenotypes, including elemental and isotopic composition. Climatic factors are known to often moderate predator effects on prey abundance, but few studies consider the combined effects of climate and predators on prey phenotype. We examined how altered precipitation moderates the effects of predators on the abundance and the chemical composition of prey, as well as the indirect effects on the basal resource: leaf litter coated in biofilm. Using an experiment with an invertebrate food web module from tank bromeliads, we manipulated the presence of an odonate predator under scenarios of 10-fold decreased, ambient, and threefold increased precipitation and measured responses of prey and their basal resource. Predators reduced prey abundance while precipitation did not. Both precipitation and predators, either singly or interactively, affected the elemental composition of prey. Predators increased C:N ratios of detritivorous beetles under high precipitation, but reduced the C:N ratio of the basal resource. Precipitation reduced the N content of filter-feeding mosquitoes. The observed changes in chemical composition may reflect physiological or developmental responses to stress imposed by both predators and drought. This study demonstrates that the impact of predators and precipitation can vary substantially across a food web, including additive and synergistic effects, and numerical and phenotypic responses.
Resumen
es Los depredadores afectan las comunidades ecologicas a través de cambios en la abundancia y fenotipo de las pesas, incluyendo la composición de elementos e isotopica. Se sabe que las variables climaticas regulan el efecto del depredador sobre la abundancia de las presas, pero pocos estudios han considerado el efecto combinado del clima y la depredación sobre el fenotipo de las presas. Se evaluó cómo cambios en la precipitación regulan los efectos del depredador sobre la abundancia y composición química de las presas, así como los efectos indirectos sobre el recurso base, la biopelícula de la hojarasca. Se realizó un experimento utilizando la red trófica de invertebrados de las bromelias tanque, se manipuló la presencia de un depredador odonato bajo los escenarios de disminución de 10 veces la precipitación, ambiental e incremento de 3 veces la precipitación y se midió la respuesta de las presas y el recurso base. El depredador pero no la precipitación redujó la abundancia de las presas; ambos, la precipitación y el depreddor, solo o en interacción afectaron la composición química de las presas. El depredador incrementó la relación C:N de los coleópteros detritivos bajo el tratamiento de precipitación alta pero redujó la relación C:N del recurso base. La precipitación redujo el contenido de N de los mosquitos. Los cambios observados en la composición quimica pueden reflejar las respuestas fisiológicas y de desarrollo al estrés impuesto por el depredador y la sequía. Este estudio demostró que el impacto del depredador y la precipitación pueden variar sustancialmente a través de la red trofica incluyendo efetos aditivos y sinérgicos y respuestas numéricas y fenotipicas.
The dynamics of interactions amongst natural enemies are central to the investigation of insect pest ecology. Ternary and quaternary interactions between parasitoids and predators in the presence of entomophagous organisms are yet to be comprehensively explored. We investigated the performance of a clone of green peach aphid ( Myzus persicae (Sulzer); Hemiptera: Aphididae), raised on savoy cabbage ( Brassica oleracea Linnaeus; Brassicaceae), under all possible combinations of: I) the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae); II) the predator Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae); III) the predator Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae); and IV) the spider Parasteatoda tepidariorum (Koch) (Araneae: Theridiidae). We demonstrate a considerably differential green peach aphid abundance, polyphenism, and fine-scale spatial distribution in response to the combination, number, and identity of the present enemy species and their interactions. Surprisingly, certain combinations led to thriving green peach aphid populations due to interference between enemies; whereas, other combinations resulted in tangible collective suppression of the population. At the frontier of agroecology and entomology, we provide fresh insights on the effects of conflict and synergy between natural enemies sharing a pest of a cash crop as prey, highlighting the consequences of the presence of a novel synanthropic spider, as a top predator, on pest regulation.
Phloem-feeding insects strive to offset the disadvantageous effects of stressors to sustain their offspring and survive. Adaptive responses to environmental stress are not well understood under complex influences of companion planting, natural enemies, and host gradient. In this study, under predation by lacewing Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), we survey the responses of green peach aphid Myzus persicae Sulzer (Hemiptera: Aphididae), reared on different densities of cabbage Brassica oleracea L. (Brassicales: Brassicaceae) to its shallot companion Allium cepa (L.) var. aggregatum G. Don (Asparagales: Amaryllidaceae). Firstly, aphid aggregative abundance was strongly influenced by shallot perturbation, predator presence and changes in cabbage-host biomass, altering aphid phenotypic plasticity. Interestingly, the shallot and predation negative impacts can be of similar magnitudes. Secondly, changes in the cabbage-host availability and biomass, especially under predation, had a strong impact on aphid traits. Our study underscores the benefits of including shallots as crop-companions in augmenting pest control, but also suggests that the outcome of coupling companion planting with natural enemies is context-dependent and thus should be empirically applied. At the confluence of ecology and agronomy, this work provides insights on how manipulated functional biodiversity may function as an alternative strategy for pestilent herbivory management in model and green-house systems.
Maximizing plant defensive strategies is integral to effective integrated pest management. Direct defenses, in the form of chemical and morphological components that inhibit pest damage, underlie host plant resistance, while indirect defenses including food provisioning and semiochemical production, improve biological control. Interactions between the two defensive strategies may be disruptive, complementary, or synergistic and are an important consideration for effective pest management programs. Glandular trichomes are plant structures that inhibit or entrap arthropods, protecting plants against herbivores, potentially at the cost of reducing natural enemy efficacy. Glandular trichomes may also contribute to indirect defense, as predatory arthropods adapted to “sticky” surfaces scavenge on entrapped arthropods. Scavenging increases predator abundance and reduces plant damage; this protective mutualism has been demonstrated with multiple sticky wild flowers but has not been assessed in an economically important plant, such as tobacco. We augmented dead arthropods (carrion) on tobacco plants grown under conditions similar to commercial production and assessed tri-trophic interactions. Carrion augmentation increased predator abundance, reduced damage to reproductive structures, and increased leaf yield, but did not reduce pest densities. We determined that systemic insecticide use did not affect carrion entrapment on tobacco plants. Review of the literature revealed that a variety of economically important plants entrap arthropods on their surfaces, indicating this mutualism has potential for development into a conservation biological control tactic.
Habitat management involving manipulation of farmland vegetation can exert direct suppressive effects on pests and promote natural enemies. Advances in theory and practical techniques have allowed habitat management to become an important subdiscipline of pest management. Improved understanding of biodiversity-ecosystem function relationships means that researchers now have a firmer theoretical foundation on which to design habitat management strategies for pest suppression in agricultural systems, including landscape-scale effects. Supporting natural enemies with shelter, nectar, alternative prey/hosts, and pollen (SNAP) has emerged as a major research topic and applied tactic with field tests and adoption often preceded by rigorous laboratory experimentation. As a result, the promise of habitat management is increasingly being realized in the form of practical worldwide implementation. Uptake is facilitated by farmer participation in research and is made more likely by the simultaneous delivery of ecosystem services other than pest suppression. Expected final online publication date for the Annual Review of Entomology Volume 62 is January 07, 2017. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Sustainable and resilient agricultural systems are needed to feed and fuel a growing human population. However, the current model of agricultural intensification which produces high yields has also resulted in a loss of biodiversity, ecological function, and critical ecosystem services in agricultural landscapes. A key consequence of agricultural intensification is landscape simplification, where once heterogeneous landscapes contain increasingly fewer crop and non-crop habitats. Landscape simplification exacerbates biodiversity losses which leads to reductions in ecosystem services on which agriculture depends. In recent decades, considerable research has focused on mitigating these negative impacts, primarily via management of habitats to promote biodiversity and enhance services at the local scale. While it is well known that local and landscape factors interact, modifying overall landscape structure is seldom considered due to logistical constraints. I propose that the loss of ecosystem services due to landscape simplification can only be addressed by a concerted effort to fundamentally redesign agricultural landscapes. Designing agricultural landscapes will require that scientists work with stakeholders to determine the mix of desired ecosystem services, evaluate current landscape structure in light of those goals, and implement targeted modifications to achieve them. I evaluate the current status of landscape design, ranging from fundamental ecological principles to resulting guidelines and socioeconomic tools. While research gaps remain, the time is right for ecologists to engage with other disciplines, stakeholders, and policymakers in education and advocacy to foster agricultural landscape design for sustainable and resilient biodiversity services.
Although predators and floral herbivores can potentially decrease plant fitness by changing pollinator behaviors, studies comparing the strength of these factors as well as their additive and interactive effects on pollinator visitation and plant fitness have not been conducted. In this study, we manipulated the floral symmetry and predator presence (artificial crab spiders) on the flowers of the shrub Rubus rosifolius (Rosaceae) in a 2 × 2 factorial randomized block design. We found that asymmetry and predators decreased pollinator visitation (mainly hymenopterans), and overall these factors did not interact (additive effects). The effect of predation risk on pollinator avoidance behavior was 62 % higher than that of floral asymmetry. Furthermore, path analyses revealed that only predation risk cascaded down to plant fitness, and it significantly decreased fruit biomass by 33 % and seed number by 28 %. We also demonstrated that R. rosifolius fitness is indirectly affected by visiting and avoidance behaviors of pollinators. The strong avoidance behavioral response triggered by predation risk may be related to predator pressure upon flowers. Although floral asymmetry caused by herbivory can alter the quality of resources, it should not exert the same evolutionary pressure as that of predator-prey interactions. Our study highlights the importance of considering simultaneous forces, such as predation risk and floral asymmetry, as well as pollinator behavior when evaluating ecological processes involving mutualistic plant-pollinator systems.
Top-down control by spider predators on grasshopper herbivores can produce trophic cascades, which may enhance plant biomass and alter plant community composition. These trophic level effects may be the result of either predator reduction in prey numbers (i.e., consumptive effects) or decreased prey foraging time in response to predator presence (i.e., non-consumptive effects). However, predator-prey interactions can be context dependent and do not always affect the plant trophic level. We conducted a field and laboratory experiment in a Northern Wisconsin (USA) old field ecosystem to uncover whether consumptive or non-consumptive effects of spider predation on grasshopper herbivores result in a trophic cascade, and if so to determine the underlying mechanisms that drive these trophic cascades. In a field experiment, four treatments examined the effects of multiple trophic-level interactions on plant biomass: 1) control treatment of vegetation only, 2) a two trophic-level interaction (grasshoppers and vegetation), and two different three trophic-level interactions: 3) the presence of “predator spiders” to examine consumptive effects, and 4) “risk spiders” with their chelicerae disarmed with beeswax to examine non-consumptive effects. In addition, a lab experiment was conducted to examine behavioral responses by grasshoppers in the presence of both an armed-spider predator and a risk spider to assess whether food quality (high vs low C:N ratios) had an effect on this interaction. Both risk and predator spiders decreased the impact of grasshoppers on plant biomass in the field experiment, and equally reduced overall grasshopper survival, indicating a non-consumptive effect. At the behavioral level, grasshoppers exhibited anti-predator behavior at the expense of reduced food intake. Food quality had no effect on the survival of grasshoppers as foraging was sacrificed for predator avoidance. Taken together, our results indicate that the resulting trophic cascade was the result of non-consumptive effects and that spider presence alone may reduce grasshopper herbivory rates.
Predators can affect prey indirectly by eliciting changes in behavior, morphology, and life history. These
nonconsumptive effects are often mediated by predator cues used by prey to avoid capture. However, predator cues can cause stress responses in prey that negatively impact survival and reproduction. We explored responses of the wolf spider Pardosa milvina (Hentz 1844) to cues from the larger wolf spider Tigrosa helluo (Walckenaer 1837) and the ground beetle Scarites quadriceps Chaudoir 1843. We exposed Pardosa to cues from both predators and measured changes in body size, weight, consumption, and lifespan. We found significant effects of predator cues only on female longevity: females exposed to Tigrosa cues had shorter lifespans than those exposed to cues from Scarites. The lack of treatment effects on energy intake suggests that predator cues act through physiological pathways. Future experiments may uncover opposing
hormonal mechanisms underlying the observed differences in lifespan.
Predators can indirectly enhance plant performance via herbivore suppression, with both prey consumption and changes in prey traits (e.g. changes in foraging behaviour) contributing to the reduction in herbivory. We performed a field experiment to determine the extent of such non-consumptive effects which consisted of repeatedly placing spiders (Pisaura mirabilis) on enclosed plants (Urtica dioica) for cue deposition. Control plants were enclosed in the same way but without spiders. After cue deposition, the enclosures were removed to allow arthropods to colonize the plants and feed on them. Arthropods were removed from the plants before the subsequent spider deposition or control enclosure. During six cycles of enclosure, we quantified leaf damage on the plants. After a seventh cycle, the colonizing arthropods were sampled to determine community composition in relation to the presence/absence of spider cues. We found that the presence of chemotactile spider cues reduced leaf damage by 50 %. In addition, spider cues led to changes in the arthropod community: smaller spiders avoided plants with spider cues. In contrast, the aphid-tending ant Myrmica rubra showed higher recruitment of workers on cue-bearing plants, possibly to protect aphids. Our results show that the risk of spider predation can reduce herbivory on wild plants and also demonstrate that non-consumptive effects can be particularly strong within the predator guild.
Predators can affect prey in two ways-by reducing their density (consumptive effects) or by changing their behavior, physiology or other phenotypic traits (non-consumptive effects). Understanding the cues and sensory modalities prey use to detect predators is critical for predicting the strength of non-consumptive effects and the outcome of predator-prey encounters. While predator-associated cues have been well studied in aquatic systems, less is known about how terrestrial prey, particularly insect larvae, detect their predators. We evaluated how Colorado potato beetle, Leptinotarsa decemlineata, larvae perceive predation risk by isolating cues from its stink bug predator, the spined soldier bug, Podisus maculiventris. When exposed to male "risk" predators that were surgically manipulated so they could hunt but not kill, beetles reduced feeding 29 % compared to controls. Exposure to risk females caused an intermediate response. Beetles ate 24 % less on leaves pre-exposed to predators compared to leaves never exposed to predators, indicating that tactile and visual cues are not required for the prey's response. Volatile odor cues from predators reduced beetle feeding by 10 % overall, although male predators caused a stronger reduction than females. Finally, visual cues from the predator had a weak effect on beetle feeding. Because multiple cues appear to be involved in prey perception of risk, and because male and female predators have differential effects, beetle larvae likely experience tremendous variation in the information about risk from their local environment.
1. Bee behaviour when visiting flowers is mediated by diverse chemical cues and signals, from the flower itself and from previous visitors to the flower. Flowers recently visited by bees and hoverflies may be rejected for a period of time by subsequent bee visitors.
2. Nectar-thieving ants also commonly visit flowers and could potentially influence the foraging decisions of bees, through the detection of ant trail pheromones or footprint hydrocarbons.
3. Here we demonstrate that, while naÏve bumblebees in laboratory trials are not inherently repelled by ant scent marks, they can learn to use them as informative signals while foraging on artificial flowers.
4. To test for similar activity in the wild, visitor behaviours at the flowers of Digitalis purpurea Linnaeus, Bupleurum fruticosum Linnaeus, and Brassica juncea (Linnaeus) Czernajew were compared between flowers that had been in contact with ants and those that had not. No differences were found between the two treatments.
5. The use of chemical foraging cues by bees would appear to be strongly dependent on previous experience and in the context of these plant species bees did not associate ant scent mark cues with foraging costs.
Prey organisms evolved a multitude of plastic responses to avoid being eaten by predators. Besides the evolution of plastic morphological responses to escape predation, prey also evolved a set of physiological stress responses to avoid dying because of chronic predator stress per se due to disruption of cellular homeostasis. As physiological stress theory predicts increased energy consumption and the inhibition of essential nonemergency body functions, we tested whether chronic predation risk may increase oxidative damage thereby generating negative effects on escape performance. Specifically, we evaluated whether predation risk reduces escape swimming speed in damselfly larvae and whether this operates through stress-associated increases in oxidative damage. Counterintuitively and in contrast with many empirical studies, chronic predation risk decreased escape performance. This is however entirely consistent with the expectation of it being a long-term cost of responding to predation risk (e.g. by increasing respiration or upregulating the stress protein levels). The decreased swimming speed could be explained by an increased oxidative damage to proteins, thereby providing one of the poorly studied ecological links between oxidative damage and whole-animal performance. This likely widespread, understudied cost of chronic predation risk may provide an important pathway of non-consumptive predator effects on prey population dynamics. Moreover, it could play an evolutionary role by acting as a selective force causing prey organisms to adjust the magnitude of the physiological stress response and should be considered when evaluating life history trade-offs thought to be mediated by oxidative damage.
Herbivores are squeezed between the two omnipresent threats of variable food quality and natural enemy attack, but these two factors are not independent of one another. The mechanisms by which organisms navigate the dual challenges of foraging while avoiding predation are poorly understood. We tested the effects of plant defense and predation risk on herbivory in an assemblage of leaf-chewing insects on Solanum lycopersicum (tomato) that included two Solanaceae specialists (Manduca sexta and Leptinotarsa decemlineata) and one generalist (Trichoplusia ni). Defenses were altered using genetic manipulations of the jasmonate phytohormonal cascade, whereas predation risk was assessed by exposing herbivores to cues from the predaceous stink bug, Podisus maculiventris. Predation risk reduced herbivore food intake by an average of 29% relative to predator-free controls. Interestingly, this predator-mediated impact on foraging behavior largely attenuated when quantified in terms of individual growth rate. Only one of the three species experienced lower body weight under predation risk and the magnitude of this effect was small (17% reduction) compared with effects on foraging behavior. Manduca sexta larvae, compensated for their predator-induced reduction in food intake by more effectively converting leaf tissue to body mass. They also had higher whole-body lipid content when exposed to predators, suggesting that individuals convert energy to storage forms to draw upon when risk subsides. In accordance with expectations based on insect diet breadth, plant defenses tended to have a stronger impact on consumption and growth in the generalist than the two specialists. These data both confirm the ecological significance of predators in the foraging behavior of herbivorous prey and demonstrate how sophisticated compensatory mechanisms allow foragers to partially offset the detrimental effects of reduced food intake. The fact that these mechanisms operated across a wide range of plant resistance phenotypes suggests that compensation is not always constrained by reduced food quality.
Predators can reduce bee pollination and plant fitness through successful predation and non-consumptive effects. In honey bees, evidence of predation or a direct attack can decrease recruitment dancing and thereby magnify the effects of individual predation attempts at a colony level. However, actual predation attempts and successes are relatively rare. It was not known if a far more common event, just detection of a predator, could inhibit recruitment. We began by testing honey bees' avoidance of the praying mantis (Tenodera sinensis). Larger predators (later mantis instars, ≥4.5 cm in body length) elicited significantly more avoidance (1.3 fold) than smaller mantis instars. Larger instars also attempted to capture honey bees significantly more often than did smaller instars. Foragers could detect and avoid mantises based upon mantis odor (74% of bees avoided an odor extract) or visual appearance (67% avoided a mantis model). Finally, foragers decreased recruitment dancing by 1.8 fold for a food source with a live adult mantis, even when they were not attacked. This reduction in recruitment dancing, elicited by predator presence alone, expands our understanding of predator non-consumptive effects and of cascading ecosystem effects for plants served by an important generalist pollinator.
Because predation risk typically alters how prey forage for food, interactions between predation risk and food availability are commonly found. Less is known about how host plant quality and predation risk interact to affect prey behaviour and physiology.Using the caterpillar, Manduca sexta, and its predator, Podisus maculiventris, the effects of predation risk and host plant quality on caterpillar feeding, growth, assimilation efficiency, and resting metabolic rate were tested.Overall, caterpillars on low-resistance tomato plants (jasmonate-insensitive) gained 14% more mass than caterpillars on high-resistance plants (wild-type tomato). On low-resistance plants, the presence of predators caused caterpillars to eat 32% less, but they gained the same mass as unthreatened caterpillars (i.e. a 19% increase in assimilation efficiency). In addition, caterpillars showed a 17% increase in resting metabolic rate in the presence of predators. On high-resistance plants, predation risk caused a decrease in feeding, but did not alter assimilation efficiency or resting metabolic rate.The reduction in physiological responses to predation risk on high- versus low-resistance plants demonstrates a tradeoff between the ability to respond to predation risk and the ability to grow, especially on well-defended plants.
Abstract Ants on flowers can disrupt pollination by consuming rewards or harassing pollinators, but it is difficult to disentangle the effects of these exploitative and interference forms of competition on pollinator behavior. Using highly rewarding and quickly replenishing artificial flowers that simulate male or female function, we allowed bumblebees (Bombus impatiens) to forage (1) on flowers with or without ants (Myrmica rubra) and (2) on flowers with or without ant scent cues. Bumblebees transferred significantly more pollen analogue both to and from ant-free flowers, demonstrating that interference competition with ants is sufficient to modify pollinator foraging behavior. Bees also removed significantly less pollen analogue from ant-scented flowers than from controls, making this the first study to show that bees can use ant scent to avoid harassment at flowers. Ant effects on pollinator behavior, possibly in addition to their effects on pollen viability, may contribute to the evolution of floral traits minimizing ant visitation.
For organisms lacking parental care and where larval dispersal is limited, oviposition site selection decisions are critical fitness-enhancing choices. However, studies usually do not consider the interdependence of the two. In this study, we evaluated the effect of food level on the oviposition behavior of Aedes albopictus (Skuse) in the presence or the absence of a nonlethal predator (caged dragonfly nymph). We also attempted to quantify the perceived cost of predation to ovipositioning mosquitoes. Mosquitoes were presented with oviposition cups containing four levels of larval food (fermented leaf infusion) with or without a caged libellulid nymph. By titrating larval food, we estimated the amount of food needed to attract the female mosquito to oviposit in the riskier habitat. As expected, oviposition rate increased with food level and decreased in the presence of a predator. However, the effect of food level did not differ between predator treatments. By calculating the difference in the amount of food for points of equal oviposition rate in the predator-present and predator-absent regression lines, we estimated the cost of predation risk to be 1950 colony-forming-units per milliliter. Our study demonstrated the importance of considering the possible interdependence of predation risk and food abundance for oviposition-site-seeking insects. This study also quantified the perceived cost of predation and found it to be relatively low, a fact with positive implications for biological control.
Aphids increase production of winged individuals as a generalized response to multiple threats, including predators, competitors, and poor host plant quality. While wing formation in response to these individual threats is well documented, few investigations have evaluated whether combined threats lead to additive or non-additive outcomes. We tested the interactive effects of predation risk and plant quality on population growth and wing induction in the potato aphid, Macrosiphum euphorbiae. Plant quality was varied using phytohormonal manipulations of tomato (Solanum lycopersicum) to elevate or suppress the jasmonate and salicylate defense pathways. Predation risk was altered by exposing aphids to lethal or risk (unable to feed) individuals of the convergent lady beetle, Hippodamia convergens. Phytohormonal treatments resulted in >4-fold variation in aphid population growth and thus strongly affected plant quality; however, the percentage of winged individuals was no different across plant types. Predators similarly reduced aphid abundance, but also elicited a ~3-fold increase in wing formation, an effect that was similar in magnitude when comparing lethal with risk predators. The overall impact of plants and predators on aphids was largely additive, an outcome that was unexpected given the likelihood for interactions between these two factors and our prior results with other herbivores in this system. We discuss this discrepancy in the context of phenotypic plasticity, non-lethal predator effects, and the ecological challenges faced by wing dimorphic insects.
Fear can have strong ecosystem effects by giving predators a role disproportionate to their actual kill rates. In bees, fear is shown through foragers avoiding dangerous food sites, thereby reducing the fitness of pollinated plants. However, it remains unclear how fear affects pollinators in a complex natural scenario involving multiple predator species and different patch qualities. We studied hornets, Vespa velutina (smaller) and V. tropica (bigger) preying upon the Asian honey bee, Apis cerana in China. Hornets hunted bees on flowers and were attacked by bee colonies. Bees treated the bigger hornet species (which is 4 fold more massive) as more dangerous. It received 4.5 fold more attackers than the smaller hornet species. We tested bee responses to a three-feeder array with different hornet species and varying resource qualities. When all feeders offered 30% sucrose solution (w/w), colony foraging allocation, individual visits, and individual patch residence times were reduced according to the degree of danger. Predator presence reduced foraging visits by 55-79% and residence times by 17-33%. When feeders offered different reward levels (15%, 30%, or 45% sucrose), colony and individual foraging favored higher sugar concentrations. However, when balancing food quality against multiple threats (sweeter food corresponding to higher danger), colonies exhibited greater fear than individuals. Colonies decreased foraging at low and high danger patches. Individuals exhibited less fear and only decreased visits to the high danger patch. Contrasting individual with emergent colony-level effects of fear can thus illuminate how predators shape pollination by social bees.
The elk or wapiti (Cervus elaphus) and bison (Bison bison) of Yellowstone National Park have lived in an environment free of wolves (Canis lupus) for the last 50 years. In the winter of 1994-1995, wolves were reintroduced into parts of Yellowstone National Park. Foraging theory predicts that elk and bison would respond to this threat by in - creasing their vigilance levels. We tested this prediction by comparing vigilance levels of elk and bison in areas with wolves with those of elk still in "wolf-free" zones of the Park. Male elk and bison showed no response to the reintro- duction of wolves, maintaining the lowest levels of vigilance throughout the study (≈12 and 7% of the time was spent vigilant, respectively). Female elk and bison showed significantly higher vigilance levels in areas with wolves than in areas without wolves. The highest vigilance level (47.5 ± 4.1%; mean ± SE) was seen by the second year for female elk with calves in the areas with wolves and was maintained during the subsequent 3 years of the study. As wolves ex- panded into non-wolf areas, female elk with and without calves in these areas gradually increased their vigilance levels from initially 20.1 ± 3.5 and 11.5 ± 0.9% to 43.0 ± 5.9 and 30.5 ± 2.8% by the fifth year of the study, respectively. We discuss the possible reasons for the differences seen among the social groups. We suggest that these behavioural re- sponses to the presence of wolves may have more far-reaching consequences for elk and bison ecology than the actual killing of individuals by wolves. 1409
While there is increasing interest in non-consumptive effects of predators on prey, physiological effects are understudied. While physiological stress responses play a crucial role in preparing escape responses, the increased metabolic rates and shunting of energy away from other body functions, including antioxidant defence, may generate costs in terms of increased oxidative stress. Here, we test whether predation risk increases oxidative damage in Enallagma cyathigerum damselfly larvae. Under predation risk, larvae showed higher lipid peroxidation, which was associated with lower levels of superoxide dismutase, a major antioxidant enzyme in insects, and higher superoxide anion concentrations, a potent reactive oxygen species. The mechanisms underlying oxidative damage are likely to be due to the shunting of energy away from antioxidant defence and to an increased metabolic rate, suggesting that the observed increased oxidative damage under predation risk may be widespread. Given the potentially severe fitness consequences of oxidative damage, this largely overlooked non-consumptive effect of predators may be contributing significantly to prey population dynamics.
Predation risk" and "fear" are concepts well established in animal behavior literature. We expand these concepts to develop the model of the "landscape of fear". The landscape of fear represents relative levels of predation risk as peaks and valleys that reflect the level of fear of predation a prey experiences in different parts of its area of use. We provide observations in support of this model regarding changes in predation risk with respect to habitat types, and terrain characteristics. We postulate that animals have the ability to learn and can respond to differing levels of predation risk. We propose that the landscape of fear can be quantified with the use of well documented existing methods such as giving-up densities, vigilance observations, and foraging surveys of plants. We conclude that the landscape of fear is a useful visual model and has the potential to become a unifying ecological concept.
Predation has immediate consequences for prey fitness and early assessment of predation risk may be advantageous for prey. We investigated the ability of the bird cherry-oat aphid, Rhopalosiphum padi (L.), to detect one of its important predators, seven spot ladybird, Coccinella septempunctata L., via chemicals in the predator’s walking track. Ladybird tracks left on leaves elicited avoidance and reduced host plant settling in aphids via contact and olfactory cues or a combination of both. Aphid avoidance behavior was dependent on ladybird sex and number of individuals, with the odor of a single ladybird eliciting attraction and the odor of several ladybirds causing avoidance. This suggests that aphids may be able to assess the risk of predation via the extent of the chemical tracks and adjust their behavioral response accordingly. Aphid responses to ladybird tracks decreased with the age of the track, potentially preventing aphids from avoiding plants on which predators have not been recently active. This avoidance mechanism may play an important role in the biological control exerted by predatory ladybirds on aphid populations.
The role of predators in food webs extends beyond their ability to kill and consume prey. Such trait-mediated effects occur when signals of the predator influence the behaviour of other animals. Because all spiders are silk-producing carnivores, we hypothesized that silk alone would signal other arthropods and enhance non-lethal effects of spiders. We quantified the herbivory inflicted by two beetle species on green bean plants (Phaseolus vulgaris) in the presence of silkworm silk and spider silk along with no silk controls. Single leaflets were treated and enclosed with herbivores in the laboratory and field. Another set of leaflets were treated and left to experience natural herbivory in the field. Entire plants in the field were treated with silk and enclosed with herbivores or left exposed to herbivory. In all cases, the lowest levels of herbivory occurred with spider silk treatments and, in general, silkworm silk produced intermediate levels of leaf damage. These results suggest that silk may be a mechanism for the trait-mediated impacts of spiders and that it might contribute to integrated pest management programmes.
Most organisms face the problem of foraging and maintaining growth while avoiding predators. Typical animal responses to predator exposure include reduced feeding, elevated metabolism, and altered development rate, all of which can be beneficial in the presence of predators but detrimental in their absence. How then do animals balance growth and predator avoidance? In a series of field and greenhouse experiments, we document that the tobacco hornworm caterpillar, Manduca sexta, reduced feeding by 30-40% owing to the risk of predation by stink bugs, but developed more rapidly and gained the same mass as unthreatened caterpillars. Assimilation efficiency, extraction of nitrogen from food, and percent body lipid content all increased during the initial phase (1-3 d) of predation risk, indicating that enhanced nutritional physiology allows caterpillars to compensate when threatened. However, we report physiological costs of predation risk, including altered body composition (decreased glycogen) and reductions in assimilation efficiency later in development. Our findings indicate that hornworm caterpillars use temporally dynamic compensatory mechanisms that ameliorate the trade-off between predator avoidance and growth in the short term, deferring costs to a period when they are less vulnerable to predation.
Fear Itself
A direct connection exists between aboveground communities and belowground soil microbiota: Soil microbes break down detrital inputs from above. Generally, it has been assumed that this relationship is largely driven by the soil community and the quality of the unconsumed plant-matter that makes up the majority of detritus in most ecosystems. However, Hawlena et al. (p. 1434 ) found that grasshoppers exposed to the threat of spider predation have an altered carbon to nitrogen ratio. When these grasshopper carcasses were subsequently integrated into the plant litter, they significantly slowed the decomposition rate, although there was no impact on the rate of decomposition of the grasshoppers themselves. Thus, the mere presence of predators, and the stress they impose, can have cascading trophic impacts and even influence the process of decomposition.
Predation is a central feature of ecological communities. Most theoretical and empirical studies of predation focus on the consequences of predators consuming their prey. Predators reduce prey population densities through direct consumption (a density- mediated interaction, DMI), a process that may indirectly affect the prey's resources, com- petitors, and other predators. However, predators can also affect prey population density by stimulating costly defensive strategies. The costs of these defensive strategies can include reduced energy income, energetic investment in defensive structures, lower mating success, increased vulnerability to other predators, or emigration. Theoretical and empirical studies confirm the existence of these induced costs (trait-mediated interactions, TMIs); however, the relative importance of intimidation (TMI) and consumption (DMI) effects remains an open question. We conducted a meta-analysis assessing the magnitude of both TMIs and DMIs in predator-prey interactions. On average, the impact of intimidation on prey de- mographics was at least as strong as direct consumption (63% and 51% the size of the total predator effect, respectively). This contrast is even more pronounced when we consider the cascading effects of predators on their prey's resources: density effects attenuated through food chains, while TMIs remained strong, rising to 85% of the total predator effect. Predators can thus strongly influence resource density even if they consume few prey items. Finally, intimidation was more important in aquatic than terrestrial ecosystems. Our results suggest that the costs of intimidation, traditionally ignored in predator-prey ecology, may actually be the dominant facet of trophic interactions.
Strong effects of predator chemical cues on prey are common in aquatic and marine ecosystems, but are thought to be rare in terrestrial systems and specifically for arthropods. For ants, herbivores are hypothesized to eavesdrop on ant chemical communication and thereby avoid predation or confrontation. Here I tested the effect of ant chemical cues on herbivore choice and herbivory. Using Margaridisa sp. flea beetles and leaves from the host tree (Conostegia xalapensis), I performed paired-leaf choice feeding experiments. Coating leaves with crushed ant liquids (Azteca instabilis), exposing leaves to ant patrolling prior to choice tests (A. instabilis and Camponotus textor) and comparing leaves from trees with and without A. instabilis nests resulted in more herbivores and herbivory on control (no ant-treatment) relative to ant-treatment leaves. In contrast to A. instabilis and C. textor, leaves previously patrolled by Solenopsis geminata had no difference in beetle number and damage compared to control leaves. Altering the time A. instabilis patrolled treatment leaves prior to choice tests (0-, 5-, 30-, 90-, 180-min.) revealed treatment effects were only statistically significant after 90- and 180-min. of prior leaf exposure. This study suggests, for two ecologically important and taxonomically diverse genera (Azteca and Camponotus), ant chemical cues have important effects on herbivores and that these effects may be widespread across the ant family. It suggests that the effect of chemical cues on herbivores may only appear after substantial previous ant activity has occurred on plant tissues. Furthermore, it supports the hypothesis that herbivores use ant chemical communication to avoid predation or confrontation with ants.
We define 'enemy free space' as ways of living that reduce or eliminate a species' vulnerability to one or more species of natural enemies. Many aspects of species' niches, in ecological and evolutionary time have apparently been moulded by interactions with natural enemies for enemy free space. We review a large number of examples. Yet many ecologists continue to think and write as though classical resource based competition for food or space is the primary determinant of species' niches. Often it is not. The recognition that the struggle for enemy free space is an important component of many species' ecologies may have important consequences for studies of community convergence, limits to species packing, and the ratio of predator species to prey species in natural communities. © 1984.
There is increasing evidence that chemical cues play a pivotal role in host selection by the natural enemies of aphids. We use Vinson's (1976) division of the host selection process into habitat location, host location and host acceptance for both parasitoids and predators and review what is known about the role of semiochemicals in aphid selection by natural enemies. For habitat location (i.e. detection of the host plant), volatiles emitted by plants after aphid attack have been described for a number of plant-aphid interactions. These synomones indicate not only the presence of an aphid host plant to the predator or parasitoid, but also the presence of aphids. Volatiles emitted from undamaged host plants are often attractive to aphid parasitoids, but less so for predators. Host location by the natural enemy on the food plant is guided by semiochemicals that mostly originate from the aphids, in particular aphid alarm pheromone, honeydew, or the smell of the aphid itself. Host acceptance is guided by contact chemicals for both predators and parasitoids. In parasitoids, host recognition may be based on visual cues or on contact chemicals on the aphid's cuticle, whereas host acceptance is ultimately based on as yet unknown substances within the aphid's hemolymph. While it appears that many predators and parasitoids are attracted to the same semiochemicals, synergistic and antagonistic interactions among chemical substances have only rarely been investigated. More research into model systems is needed, not only to identify important semiochemicals, but also to determine their range of attraction. Recent progress in the development of analytical techniques has created new opportunities to improve our understanding of the chemical ecology of aphid-natural enemy interactions in the coming years.
Indirect effects emerge when a change in the abundance of one species indirectly affects another by changing the abundances of intermediate species—called density‐mediated indirect effects—or they arise when one species modifies how two other species interact—called trait‐mediated indirect effects. I report on field experiments that evaluated how grass and herb biomass in old‐field interaction webs was influenced indirectly by a spider carnivore through its interactions with a generalist and a grass‐specialist grasshopper species. I manipulated interaction pathways between the spider and the plants using different combinations of the grasshopper species. I changed the modality of predator‐prey interactions to isolate density‐mediated from trait‐mediated effects using natural spiders (predation spiders) or spiders that were prevented from subduing prey by mouthpart manipulation (risk spiders). I found that indirect effects were stronger in speciose, reticulate food webs than in linear food chains owing to a trait‐mediated effect, a diet shift by herbivores in response to predation risk. Spiders alone did not have significant effects on grasshopper densities in the field experiments, removing any possibility of density‐mediated indirect effects. The study illustrates that ecologists should not underestimate the importance of behavioral ecology in determining community‐level interactions.